Hydrolyzed Organic Fish Fertilizer and Poultry Litter Influence Yield and Rhizosphere Ecology of Sweetpotato

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  • 1 College of Agriculture, Environment and Nutrition Sciences and G. W. Carver Agricultural Experiment Station, Tuskegee University, Tuskegee AL 36088

Organic fertilization techniques have become an attractive alternative to conventional techniques, but there remains interest in their impact on rhizosphere ecology. This study was aimed at assessing the impacts of various organic fertilizer amendments on storage root yield, chemical, biochemical, and microbial factors in the rhizosphere ecosystem and the bacterial community composition in the rhizosphere ecosystem. Four sweetpotato cultivars (J6/66, NCC-58, TU Purple, and Whatley/Loretan) and four organic fertilizer treatments [poultry litter, Megabloom (fish protein), NPK, and an untreated control] were used in the study. The experiments were conducted as a randomized complete block design with a 4 × 4 factorial treatment arrangement and three replications. Fertilizer treatments were split-applied at the rate of 134–67–67 kg·ha−1 NPK equivalent based on soil test recommendations 1 and 4 weeks after planting as single bands 15 cm from the plants and organic amendments were calculated based on total N content. Rhizosphere soil samples were collected at harvest and analyzed for soil pH, soil organic carbon (SOC), bacterial 16S rDNA, and selected soil enzymes. Organic amendments did not affect storage root yield or percent dry matter but enhanced both the mass and number of US#1 storage roots. Rhizosphere pH varied depending on cultivar and cultivar response varied with pH and ranged from 6.1 to 6.8, whereas SOC was similar regardless of the amendment. The impact of fertilizers was evident as Megabloom (fish protein) treatment suppressed the relative abundance (RA) of nitrifiers (Nitrosococcus and Nitrosomonadaceae). Also, the rhizosphere of ‘Whatley/Loretan’ seemed to have been a beneficial habitat for populations of common nitrogen-fixing bacteria Bradyrhizobium elkanii, and Rhodospirillaceae sp. as their RA increased significantly in the rhizosphere. That bacteria associated with carbon and nitrogen cycling under aerobic conditions were found to be ubiquitous in the rhizosphere of sweetpotato, suggesting that certain amendments positively impacted the populations of nitrogen-cycling bacteria, thus making them a viable alternative to NPK when considering increasing or sustaining yield while promoting long-term soil health.

Abstract

Organic fertilization techniques have become an attractive alternative to conventional techniques, but there remains interest in their impact on rhizosphere ecology. This study was aimed at assessing the impacts of various organic fertilizer amendments on storage root yield, chemical, biochemical, and microbial factors in the rhizosphere ecosystem and the bacterial community composition in the rhizosphere ecosystem. Four sweetpotato cultivars (J6/66, NCC-58, TU Purple, and Whatley/Loretan) and four organic fertilizer treatments [poultry litter, Megabloom (fish protein), NPK, and an untreated control] were used in the study. The experiments were conducted as a randomized complete block design with a 4 × 4 factorial treatment arrangement and three replications. Fertilizer treatments were split-applied at the rate of 134–67–67 kg·ha−1 NPK equivalent based on soil test recommendations 1 and 4 weeks after planting as single bands 15 cm from the plants and organic amendments were calculated based on total N content. Rhizosphere soil samples were collected at harvest and analyzed for soil pH, soil organic carbon (SOC), bacterial 16S rDNA, and selected soil enzymes. Organic amendments did not affect storage root yield or percent dry matter but enhanced both the mass and number of US#1 storage roots. Rhizosphere pH varied depending on cultivar and cultivar response varied with pH and ranged from 6.1 to 6.8, whereas SOC was similar regardless of the amendment. The impact of fertilizers was evident as Megabloom (fish protein) treatment suppressed the relative abundance (RA) of nitrifiers (Nitrosococcus and Nitrosomonadaceae). Also, the rhizosphere of ‘Whatley/Loretan’ seemed to have been a beneficial habitat for populations of common nitrogen-fixing bacteria Bradyrhizobium elkanii, and Rhodospirillaceae sp. as their RA increased significantly in the rhizosphere. That bacteria associated with carbon and nitrogen cycling under aerobic conditions were found to be ubiquitous in the rhizosphere of sweetpotato, suggesting that certain amendments positively impacted the populations of nitrogen-cycling bacteria, thus making them a viable alternative to NPK when considering increasing or sustaining yield while promoting long-term soil health.

Sweetpotato [Ipomea batatas (L.) Lam.] is a tropical root crop that belongs to the Convolvulaceae or morning glory family. It is a creeping dicotyledonous plant and an important crop, widely grown in tropical, subtropical, and warm temperate regions. It ranks the world’s seventh most important crop, with an estimated annual production of ≈122 million metric tons (Collado et al., 1999; FAO, 2005). Sweetpotato is especially valued because of its agronomic advantages for marginal lands, it is highly adaptable, and tolerates high temperatures, low fertility soil, and drought (FAO, 2010). Sweetpotato is also a nutritious vegetable with a high content of fiber, carbohydrates, and moderate iron (leaves), protein, vitamins A, B6, and C, and calcium, second only to potato (CSPI, 1992). Depending on the variety, sweetpotato has varying amounts of beta-carotene with orange-fleshed types containing more than white or cream-fleshed varieties. Purple-fleshed varieties are high in anthocyanins which have important antioxidant and anti-inflammatory properties, thus its cultivation is encouraged in developing countries where malnutrition associated health issues are high (Mortley et al., 2017; Chang et al., 2010; Choi et al., 2009; Failla et al., 2009).

Several researchers have demonstrated a wide range of effects of fertilizer, including nitrogen on storage root yield of sweetpotatoes. For example, Jet and Mulkey (1996) reported that the applying N at 50.4 kg·ha−1 21 d after transplanting produced greater yields of US#1 storage roots compared with a higher rate. Villordan et al. (2013) reported that lateral root length of storage roots increased substantially as N rates increased from 0 to 50 kg·ha−1, whereas increasing the N rates to either 100 or 200 kg·ha−1 did not result in any further increases in root growth.

Organic amendments were the primary soil amendments until the innovations and techniques of the Green Revolution (Horne, 2008). Inorganic fertilizers began to replace organic fertilizers as producers have relied on them to maintain production demands to keep pace with population growth. In addition, most N-based fertilizers are produced from fossil fuels, which have increased in price exponentially over the past decade (Wen-yuan, 2007). With increasing concerns over fertilizer pricing and reports of negative effects attributed to its use, organic fertilizers and organic practices have received renewed interest.

Organic production in the United States has grown since the inception of national organic production and labeling standards in 2002 (Baker, 2005). Several studies have shown that organic production is comparable to conventional systems in terms of yield; however, organic systems had enhanced microbial biomass and activity, increased soil organic matter, increased nutrient pools, and other soil properties (Delate et al., 2003; Klonsky, 2000). A study comparing compost with or without cover crops and tillage on organic vs. conventional sweetpotato production showed that leaf N, P, and K concentrations were greatest in the compost/cover crop combination compared with the other systems (Treadwell et al., 2008). Other studies found greater P, Mg, and Fe levels in organic systems and those mineral nutrients were on average higher in organically grown crops though results were somewhat inconclusive (Worthington, 2001).

The soil–microbial–plant system holds the capacity to sustain nutrient demands ecologically and efficiently due to the high amounts of nutrients that pass through the microbial biomass (Kennedy, 1995). Soil microorganisms drive most soil processes, such as nutrient cycling, availability, and retention; decomposition of organic materials; and soil organic matter accumulation primarily through the utilization of enzymes (Coleman et al., 2004). Alterations in the physical and chemical nature of soils may lead to shifts in the composition of the microbial community and changes in microbial function. Rhizosphere contains beneficial microorganisms that displace harmful microorganisms through aggressive colonization or through the production of plant growth hormones such as auxins and kiritin (Herman et al., 2008). The rhizosphere has a large impact on plant performance in several ways, as it not only supports the plant in the acquisition of water and nutrients, but also helps modulates the plant’s ability to cope with pathogens as well as supports high diversity of microorganisms. Studies have shown that different growth stages of plants can influence the rhizosphere microbes, due to changes in rhizodeposition. For example, young roots can supply more energy to soil microorganisms, as they produce more exudates than older roots (Bowen and Rovira, 1976; Hawes et al., 2012; Lynch and Whipps, 1990). Plant growth-promoting rhizobacteria are free-living, soil-borne bacteria that colonize the rhizosphere and, when applied to crops, enhance the growth of plants. Plant growth-promoting rhizobacteria may enhance plant growth either by direct or indirect mechanisms including nitrogen fixation (Vessey, 2003). In the past, understanding the complex diversity of soil microorganisms was limited because only a small portion of soil microbial populations can be cultured and identified using standard approaches. For instance, several studies have used soil enzymes to assess changes in soil, as soil enzymes are an essential part of microbial communities in soil systems and are strongly influenced by changes in microbial community composition (Ndiaye et al., 2000; Sun et al., 2004). The β-glucosidase (β-GLU) and N-acetyl-β-glucosaminidase (β-NAG), and phosphatase enzymes [acid phosphatase (ACP) and alkaline phosphatase (ALKP)] were used for this study because they are known to be sensitive to soil management and have been proposed as soil quality indicators because their ability to provide early indications of changes in organic matter status (Ekenler and Tabatabai, 2003; Moore-Kucera and Dick, 2008). However, use of high-throughput sequencing techniques, such as 454 pyrosequencing of 16S ribosomal RNA (rRNA) gene has allowed for the exploration of microbial communities' structure and taxonomic composition at greater depth and increased the current knowledge of soil microbial communities (Bruinsma et al., 2003; Lauber et al., 2009; Shange et al., 2012). Pyrosequencing has also been shown to detect changes in microbial communities due to organic and conventional farming and increasing current knowledge about the influence of organic amendments has on soil microbial communities (Chaudhry et al., 2012; Leff and Fierer, 2013; Li et al., 2012; Sugiyama et al., 2010; Widmer et al., 2006).

The objectives of the study were to assess the impacts of various organic fertilizer amendments on storage root yield, and chemical and biochemical factors of the rhizosphere ecosystem, and the bacterial community composition in the rhizosphere ecosystem.

Materials and Methods

The study was conducted as a randomized complete block design with a 4 × 4 factorial treatment arrangement and three replications. The treatment combinations were conventional NPK fertilizer, poultry litter, Megabloom (hydrolyzed fish protein fertilizer), and an untreated check. The sweetpotato cultivars were J6/66, NCC-58, TU Purple, and Whatley-Loretan. The soil type at the study site was Norfolk sandy loam (fine, siliceous, thermic Typic, Paleudults) with a pH of ≈5.9 and organic matter content of <1%. The field was prepared conventionally and soil samples were collected for elemental analysis at 15-cm depths. The cores were composited and analyzed by the Plant and Soil Testing Laboratory at Auburn University for mineral constituents (Ca, Mg, P, K, pH).

Treatment calculations and planting.

Treatments were split-applied at the rate of 134–67–67 kg·ha−1 NPK equivalent based on soil test recommendations 1 and 4 weeks after planting as single bands 15 cm from the plants and organic amendments were calculated based on total N content. Poultry litter, unlike commercial fertilizers, is quite variable, and according to Fulhage and Pfost (1994) can vary up to 50% based on animal sources. Available values of litter nutrients using data from Fulhage and Pfost (1994) were total N of 27 kg·ton−1, composed of 24 kg·ton−1 organic N and 3 kg·ton−1 NH4N, 29.5 kg·ton−1 P2O5, and 19 kg·ton−1 K2O. In addition, the amount of organic N available was based on days from collection to incorporation, which is 20% beyond 7 days. Calculations were based on the following equation:

crop Nresidual Navailable NH4-­N+available organic N

Ten stem cuttings of each sweetpotato cultivar were transplanted into 3-row plots 1.2 m × 3 m with an in-row spacing of 0.3 m and plants drip irrigated as needed.

Harvest and rhizosphere soil analysis.

Plants were harvested from the middle row of each plot by cutting the vines at ground level and fresh weights of foliage and storage roots were recorded. Subsamples of foliage and storage roots (US#1 grade) were dried for 72 h at 70 °C. This dry weight information was used to calculate a fresh-to-dry weight conversion factor to determine storage root dry weight. Percent dry matter (DM) [(dry weight/fresh weight) × 100] was calculated for storage roots.

Triplicate rhizosphere soil samples from each plot were taken at harvest, dried and analyzed for pH, soil organic carbon (SOC), and enzyme activity. Soil pH was determined using 1:2.5 soil/water and SOC using the wet oxidation method (Walkley and Black, 1934). Phosphomonoesterase activity was measured by the method of Tabatabai and Dick (2002); β-GLU and β-NAG activity by referenced assays (Eivazi and Tabatabai, 1977; Parham and Deng, 2000).

Whole DNA was extracted from ≈0.25g of soil (oven dry basis of field-moist soil) using the Power Soil Extraction Kit (MO BIO Laboratories, Soloana Beach, CA). Extracted DNA (2 µL) was quantified using Nanodrop ND-1000 spectrophotometer (Nanodrop Technologies, Wilmington, DE). Following extraction and quantification, the samples were then submitted to MRDNA Laboratories (Shallowater, TX) for polymerase chain reaction (PCR) optimization and sequence analysis. The 16S rRNA gene V4 variable region PCR primers 515/806 were used in a single-step 30 cycle PCR using the HotStarTaq Plus Master Mix Kit (Qiagen, Valencia, CA). Sequencing was on an Ion Torrent PGM (Roche, Brandford, CT) following the manufacturer’s guidelines. The resulting sequence data were processed using an analysis pipeline developed at MR DNA Laboratories [e.g., the removal of barcodes and primers, sequences <150 base pairs (bp) removed, sequences with ambiguous base calls and with homopolymer greater than 6 bp]. Sequences were denoised, operational taxonomic units (OTUs) generated and chimeras removed. OTUs were defined by clustering at 3% divergence (97% similarity). Final OTUs were taxonomically classified using BLASTn against a database derived from RDPII (http://rdp.cme.msu.edu) and National Center for Biotechnology Information (NCBI; www.ncbi.nlm.nih.gov). Samples are being submitted to the NCBI Sequence Read Archive. OTUs were then compiled into every taxonomic level into count files that actual number of sequences for each taxonomic classification, and the percentage files that contained the proportion percentage of sequences at each taxonomic classification for each sample.

All data were subjected to analysis of variance (ANOVA) using the general linear model procedure (SAS Institute, 2009). Treatment and cultivar means were separated by Tukey-Kramer’s test at the 0.05 level of probability.

Results and Discussion

Biomass production.

The main effect of organic amendments on storage root yield and percent DM (Table 1) show that organic amendments had no significant impact on total storage root yield or DM, but did influence the yield of US#1 storage roots. The yield of US#1 storage roots was highest for plants in which poultry litter (PL) was applied relative to that of control plants but not different from plants receiving Megabloom (fish hydrolysate) or NPK. However, plants receiving PL or Megabloom produced a greater number of US#1 storage roots compared with NPK or the control plants. Similarly, cultivar had no significant influence on total storage root yield or on the number of US#1storage roots produced (Table 2), although ‘Whatley/Loretan’ produced the highest yield of 26 t·ha−1. Organic amendments had no significant impact on DM (Table 1) and the major influence was based on variety (Table 2), with ‘TU Purple’ having the highest DM. These DM levels are consistent with these respective varieties when grown in the field.

Table 1.

The main effect of organic amendment on total storage and US#1 root yield, number of US#1 and percent dry matter (DM) of four sweetpotato cultivars.

Table 1.
Table 2.

The main effects of organic amendment on total storage and US#1 root yield, number of US#1 and percent dry matter (DM) of four sweetpotato cultivars.

Table 2.

A contrast of fertilized vs. nonfertilized plants show that on a whole, plants that received nutrient amendments produced greater yields and numbers of US#1 storage roots only while a contrast of organic vs. inorganic showed that organic amendments enhanced yield of US#1 storage roots. These results show that organic amendments exerted greater impact on yield of US#1 storage roots and number but did not influence total yield or storage root DM.

Nutrients in organic fertilizer are released through mineralization by the activity of soil microorganisms. Depending on existing soil conditions including pH and moisture status, mineralization rates can be impacted, and it is probable that the lack of total yield response to organic amendments in this study could be related in part to slower mineralization rates resulting in fewer nutrients available for plant uptake (Boyhan et al., 2010). As mineralization rates of PL have been reported as slow (Whitmore, 2007), researchers in the region have suggested applying organic fertilizer 14 to 20 d earlier than normal to compensate for slow mineralization rates. These results suggest that plant responses would be more positive in subsequent years.

Soil pH and organic carbon.

There were significant interactions between fertilizer amendments and cultivar for rhizosphere pH (Table 3). Rhizosphere pH varied depending on cultivar and cultivar response varied with pH and ranged from 6.1 to 6.8. The results suggest that the organic amendments lowered rhizosphere pH values in ‘Whatley/Loretan’ and ‘NCC-58’ treated with Megabloom and ‘TU Purple’ plots receiving PL having the lowest pH values. Cultivar influenced SOC (Table 3) in the rhizosphere and ranged from 0.63% for ‘Whatley/Loretan’ to 1.1% for ‘TU Purple’. The significantly lower SOC content in the rhizosphere of ‘Whatley/Loretan’ compared with that of the other three cultivars suggest that there might have been higher organic matter content in the rhizosphere of ‘TU Purple’, ‘NCC-58’, and ‘J6/66’ in general, as well as from decaying plant materials, slough off root hairs, and root exudates.

Table 3.

Statistical significance from analysis of variance of fertilizer amendments, cultivar and fertilizer amendments × cultivar interaction for soil pH, organic carbon, and enzyme activities.

Table 3.

Selected soil enzymes.

Generally, the fertilizer amendments influenced rhizosphere enzyme activity regardless of cultivar (Table 4). The activity of ACP increased substantially with all three fertilizer amendments relative to the control plots with the highest activity obtained in the rhizosphere of plants receiving Megabloom. On average, ACP activity increased 44% compared with those of the control plots. Results for ALKP show that there was a 3-fold increase in rhizosphere activity in plots receiving fertilizer amendments compared with the control plots. Thus, all three fertilizer amendments increased ALKP activity with NPK-treated plots having the highest. The activity of β-glucosaminidase (β-NAG) also increased in plots receiving PL, Megabloom, and NPK in relation to the control plots. The magnitude of increase in β-NAG activity ranged from 40% to 89% with PL and NPK plots having the highest activity. Even though plots treated with Megabloom had marginally lower activity relative to the other treated plots, it was still 40% greater than in control plots. Similarly, as with ALKP, all three amendments increased the activity of β-GLU 3-fold, with NPK-treated plots having the highest activity followed by Megabloom and PL-treated plots. Thus the control plots had lower enzyme activity, whereas those receiving fertilizer amendments had greater activity, suggesting that the organic amendments did not adversely affect enzyme activity relative to NPK-treated plots (Table 4).

Table 4.

Main effect of fertilizer amendments on soil enzyme activity.

Table 4.

The addition of organic amendments increased soil enzyme and microbial activity, which is consistent with what others have reported (Edmeades, 2003; Gutierrez-Miceli et al., 2007)· Further, activities of most soil enzymes increase as soil substrate increases, reflecting larger microbial communities, and increased stabilization of enzymes by humic materials (Burns, 1983). Provocation of enzymatic activity can also be a result of the release of exudates in the rhizosphere ecosystem. These exudates can thus activate the microbial synthesis of intracellular and extracellular enzymes. In contrast, the C-rich exudates can also serve as an energy source for microbial production of extracellular enzymes that increase decomposition activities (Gianfreda, 2015). In addition to exudate release and pathogen control, one of the most important functions in the bacterial community of the rhizosphere is phosphate solubilization. As this process is stewarded by bacteria and the extracellular enzymes that they produce (ACP, ALK, and more), the results showing increased activity of phosphatase enzymes substantiate the literature that soil amendments (inorganic and organic) have a stimulating impact on rhizosphere phosphatase (Ai et al., 2012).

Bacterial community composition.

In terms of the bacterial ecology, the results for the phyla and class level (Fig. 1) indicated that Proteobacteria was the most dominant phylum and class identified. When considering the class level of taxonomy (of which certain groups become more functionally evident) (Shange et al., 2012), four classes of Proteobacteria (Alphaproteobacteria, Betaproteobacteria, Deltaproteobacteria, Gammaproteobacteria), as well as the class Actinobacteria were the most prevalent in the class groups. ‘TU Purple’ and ‘Whatley/Loretan’ significantly influenced Gemmatimonadetes at every taxonomic level, suggesting that these cultivars produce root exudates that may have attracted these bacteria.

Fig. 1.
Fig. 1.

Bacterial composition at the phylum level for each sample of sweetpotato rhizosphere. 0bh to 0tu = Control ‘TU Purple’, ‘J6/66’, ‘NCC-58’, ‘Whatley’; bl = poultry litter; fsh = Magabloom (fish hydrolysate); fert = NPK fertilizer all combined with the same four sweetpotato cultivars.

Citation: HortScience horts 54, 5; 10.21273/HORTSCI13740-18

Taxonomic response to fertilizer treatment.

There were 27 genera present in the rhizosphere samples. Significant effects were observed for amendments on the populations of Flexibacter, Mycobacterium, Nitrosococcus, Nitrosomonadaceae, and Roseiflexus (Table 5). Of the 1896 species observed, 30 were in great quantities in the rhizosphere samples. The ANOVA showed that organic amendments had the greatest effect on species composition. Megabloom significantly decreased the bacterial relative abundance (RA) of Nitrosococcus, Nitrosomonadaceae, and Flexibacter genera compared with the control and the other amendments except PL, where the RA was not different for Nitrosococcus and Nitrosomonadaceae (Table 5). In contrast, Megabloom increased the populations of Mycobacterium and Rubrobacter compared with the control (Table 5). NPK increased Nitrosomonadaceae, whereas Megabloom increased the RA of Gemmatimonas, Mycobacterium, and Rubrobacter genera, and decreased the RA of Flexibacter, Nitrosococcus, Nitrosomonadaceae, and Roseiflexus genera. Thus, Megabloom continued to impact bacterial populations at the species level as it had at the genus level compared with the control. For example, Novosphingobium sp. decreased significantly compared with the control and other amendments, whereas the RA of Rhodospirillaceae sp. increased in plots receiving NPK and organic amendments compared with the control plots (Table 5). The addition of fertilizer and organic amendments had a significant impact on bacteria at every taxonomic level compared with the control; however, Megabloom and PL organic rhizosphere soils had similar or significantly different effects on RA at the genus and species taxonomy level compared with rhizosphere soils amended with inorganic fertilizers.

Table 5.

Effect of fertilizer and organic amendments on bacterial relative abundance in sweetpotato rhizosphere at the genus and species taxonomic level.

Table 5.

These results demonstrate that at the genus and species levels of taxonomy, the type of fertilizer, and the type of organic substrate influence the changes in some of the most abundant groups in the rhizosphere ecosystem. Not only are there changes to the composition of the community that seem to be functionally obtuse, there were changes to taxa that have been identified as playing important functional roles in the soil ecosystem. Nitrosomonadaceae is a family that includes Nitrosomonas, Nitrosospira, and Nitrosovibrio lithotrophic ammonia oxidizing bacteria (AOB). Nitrosococcus, another AOB from the Gammaproteobacteria class responded positively to the treatments. Although Flexibacter is well known for its fish pathogenicity (Crump et al., 2003), there have been other isolates found in soils that participate in denitrification (Wu et al., 1994). As this process requires net NO3-N availability, there may have been a lower availability of NO3-N due to the slow release of N from Megabloom (Mikkelsen and Hartz, 2008). It would be reasonable to surmise that soil Flexibacter would reduce RA in such an environment. Although PL is also a slow-release organic fertilizer, it has been stated that rates of mineralization can be highly variable (Gaskell and Smith, 2007). Further evidence to substantiate this notion is the parallel RA of the nitrifiers (Nitrosococcus and Nitrosomonadaceae). The statistical significance of RA of the nitrifying bacteria relative to the control might be due to soil environment factors. According to Wang et al. (2015), soil pH value, number of ions, NH4+, soil temperature, and organic matter content have a critical impact on the bacterial population.

Novosphingobium has the ability to degrade large aromatic rings, leading to a high diversity of environments in which they have been found, including oil-contaminated soil (Kämpfer et al., 2011), surface water sediments (Balkwill et al., 1997; Liu et al., 2005; Sohn et al., 2004), and wastewater facilities (Fujii et al., 2003; Neef et al., 1999). Only recently, this group has been discovered in plant-associated habitats such as the internal stem of Gossypium hirsutum (Kämpfer et al., 2015), the rhizosphere of Arabidopsis thaliana (Gan et al., 2013), and surface of a crown gall tumor on grapevine (Lin et al., 2014). One suggestion for Novosphingobium association with plants in the rhizosphere is the presence of xenobiotic aromatic compounds. Root exudates contain various molecules that are structurally related to aromatic xenobiotics (Ledger et al., 2012) that can potentially serve to create an ecosystem favorable to those bacteria with the ability to catabolize such compounds.

Taxonomic response to varieties.

Significant effects of cultivar were observed for Mycobacterium and Sinobacter. The population of Sinobacter increased in the rhizosphere of ‘Whatley/Loretan’ and Mycobacterium in the rhizosphere of ‘TU Purple’ compared with other cultivars (Table 6). ‘Whatley/Loretan’ significantly influenced the rhizosphere populations of Bradyrhizobium elkanii, Rhodospirillaceae sp., and Sinobacter sp. (Table 6) compared with ‘TU Purple’ and ‘J6/66’ but was not different from ‘NCC-58’.

Table 6.

Effect of cultivars on bacterial relative abundance in sweetpotato rhizosphere at the genus and species taxonomic level.

Table 6.

A significant interaction between the organic amendment and cultivar for Gemmatimonadaceae and Gemmatimonas (Table 7) and for Anaerolinaceae and Gemmatimonadaceae sp. (Table 8). Anaerolinaceae population increased significantly in the rhizosphere of ‘J6/66’ when NPK was applied compared with the control and the other amendments. Gemmatimonadaceae populations increased significantly when PL and NPK were applied compared with control. Gemmatimonadaceae significantly increased in the rhizosphere of ‘Whatley/Loretan’, when NPK was applied compared with control and the other organic amendments. Megabloom significantly decreased Gemmatimonadaceae population compared with control, NPK and PL in the rhizosphere of ‘Whatley/Loretan’, but increased significantly in the rhizosphere of ‘NCC-58’ when NPK and organic amendments were applied compared with the control (Table 8).

Table 7.

Effect of fertilization and cultivar on bacterial composition in sweetpotato rhizosphere at the genus taxonomic level.

Table 7.
Table 8.

Effect of fertilizer and organic amendments and cultivar on bacterial composition in sweetpotato rhizosphere at the species taxonomic level.

Table 8.

‘TU Purple’ and ‘Whatley/Loretan’ significantly affected the phylum Gemmatimonadetes at every taxonomical level, suggesting that these cultivars produce exudates that may attract certain bacterial groups. Bacteria belonging to this phylum are frequently detected in a variety of environments and are noted as one of the nine most common from the soil in 16S rRNA gene libraries. Janssen (2006) and Khodadad et al. (2011) also found that these bacteria are abundant in carbon-rich soils, further suggesting that these bacteria may have influenced carbon content in the rhizosphere of these two cultivars. Gemmatimonadetes play a role in phosphorus cycling (Zhang et al., 2003), as they improve phosphorus removal in wastewater, and could play a similar role in the soil. The varying RA of Rhodospirillaceae sp. among the cultivars is worthy of note, as the capacity to fix molecular nitrogen is ubiquitous among members of Rhodospirillaceae, whereas the efficacy of the process varies among species (Madigan et al., 1984). This group, along with Bradyrhizobium elkanii (another known N-fixer) was also highest in the ‘Whatley/Loretan’ rhizosphere (also lowest in SOC and highest in β-NAG activity, although not significant. The abundant concentration of the closely related Azospirillium sp. (known AOB) is interesting, as this species is well known as associative nitrogen fixers, which can partly explain the ability of sweetpotato to grow in N-deficient marginal soils (Mortley and Hill, 1990; Trotman et al., 1993).

The findings suggest that organic fertilizer and variety influenced selected microbial populations and enzymatic function within the soil rhizosphere of sweetpotato. The effects of organic amendments on bacterial composition varied as population differed significantly under the different organic amendments as bacteria involved in C and N cycling were dominant at every taxonomic level. Organic amendments had no significant impact on SOC but variety did, with soil from ‘Whatley/Loretan’ rhizosphere having lower SOC than other cultivars. Although variety did not affect enzyme activity, all amendments significantly increase ACP, ALKP, β-NAG, and β-Glu enzyme activity compared with the control, but there was no significant difference among treatment. The phyla Actinobacteria and Gemmatimonadetes were also found in the samples, which could explain the increased activity seen in β-GLU and β-glucosaminidase enzymes. Based on these findings, we gather that bacteria associated with C and N cycling under aerobic conditions can dominate in the rhizosphere of sweetpotato. Most importantly, these findings gave a better understanding of microbiome associated with sweetpotato that may not have been previously connected with this storage root crop. Not only were we able to elucidate the storage root microbiome of these particular cultivars, but also demonstrate differential responses of organic and inorganic fertilizers possibly allowing for more studies investigating alternative fertilization technology as well as nutrient uptake and the soil, plant, microbe interface.

Literature Cited

  • Ai, C., Liang, G., Sun, J., Wang, X. & Zhou, W. 2012 Response of ectracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil Geoderma 173–174 330 333

    • Search Google Scholar
    • Export Citation
  • Baker, B. 2005 Brief History of Organic Farming and the National Organic Program. In: Organic Farming Compliance Handbook. Organic Materials Review Institute, Eugene, OR

  • Balkwill, D.L., Drake, G.R., Reeves, R.H., Fredrickson, J.K., White, D.C., Ringelberg, D.B., Chandler, D.P., Romine, M.F., Kennedy, D.W. & Spadoni, C.M. 1997 Taxonomic study of aromatic degrading bacteria from deep-terrestrial-subsurface sediments and description of Sphingomonas aromaticivorans sp. nov., Sphingomonas subterranea sp. nov., and Sphingomonas stygia sp. nov Intl. J. Syst. Bacteriol. 47 191 201

    • Search Google Scholar
    • Export Citation
  • Bowen, G.D. & Rovira, A.D. 1976 Microbial colonization of plant roots Annu. Rev. Phytopathol. 114 121 144

  • Boyhan, G., Hicks, R.J., Torrance, R.L., Riner, C.M. & Hill, C.R. 2010 Evaluation of poultry litter and organic fertilizer rate and source for production of organic short-day onions HortTechnology 20 304 307

    • Search Google Scholar
    • Export Citation
  • Bruinsma, M., Kowalchuk, G.A. & Van Veen, J.A. 2003 Effects of genetically modified plants on microbial communities and processes in soil Biol. Fertil. Soils 37 329 337

    • Search Google Scholar
    • Export Citation
  • Burns, R.G. 1983 Extracellular enzyme-substrate interactions in soil, p. 249. In: J.H. Slater, R. Whittenbury, and J.W.T. Wimpenny (eds.). Microbes in their natural environment. Cambridge University Press, Cambridge, UK

  • CSPI 1992 Sweetpotato nutrition. Washington D.C. USA. 24 Mar. 2018. <http://www.foodreference.com/html/sweet-pot-nutrition.html>

  • Chang, W.H., Huang, Y.F., Yeh, T.S. & Liu, J.F. 2010 Effect of purple sweetpotato leaves consumption on exercise-induced oxidative stress, and IL-6 and HSP72 levels J. Appl. Physiol. 109 1710 1715

    • Search Google Scholar
    • Export Citation
  • Chaudhry, V., Rehman, A., Mishra, A., Chauhan, P.S. & Nautiyal, C.S. 2012 Changes in bacterial community structure of agricultural land due to long-term organic and chemical amendments Microb. Ecol. 64 450 460

    • Search Google Scholar
    • Export Citation
  • Choi, J.H., Choi, C.Y., Lee, K.J., Hwang, Y.P., Chung, Y.C. & Jeong, H.G. 2009 Hepatoprotective effects of an anthocyanin fraction from purple-fleshed sweet potato against acetaminophen-induced liver damage in mice J. Med. Food 12 320 326

    • Search Google Scholar
    • Export Citation
  • Coleman, D.C., Crossley, D.A. & Hendrix, P.F. 2004 Fundamentals of soil ecology. 2nd ed. Elsevier Inc., Burlington, VT

  • Collado, L.S., Mabesa, R.C. & Corke, H. 1999 Genetic variation in the physical properties of sweet potato starch J. Agr. Food Chem. 47 4195 4201

  • Crump, E.M., Perry, M.B., Gale, S., Crawford, E. & Kay, W.W. 2003 Lipopolysaccharide O-antigen antibody-based detection of the fish pathogen Flavobacterium psychrophilum J. Mol. Microbiol. Biotechnol. 6 182 190

    • Search Google Scholar
    • Export Citation
  • Delate, K., Duffy, M., Chase, C., Holste, A., Friedrich, H. & Wantate, N. 2003 An economic comparison of organic and conventional grain crops in a long-term agroecological research (LTAR) site in Iowa Amer. J. Altern. Agr. 18 59 69

    • Search Google Scholar
    • Export Citation
  • Edmeades, D.C. 2003 The long-term effects of manures and fertilisers on soil productivity and quality: A review Nutr. Cycl. Agroecosyst. 66 165 180

    • Search Google Scholar
    • Export Citation
  • Eivazi, F. & Tabatabai, M.A. 1977 Phosphatases in soils Soil Biol. Biochem. 9 167 172

  • Ekenler, M. & Tabatabai, M.A. 2003 Tillage and residue management effects on beta-glucosaminidase activity in soils Soil Biol. Biochem. 35 871 874

  • Failla, M.L., Thakkar, S.K. & Kim, J.Y. 2009 In vitro bioaccessibility of beta-carotene in orange fleshed sweet potato (Ipomoea batatas Lam.) J. Agr. Food Chem. 57 10922 10927

    • Search Google Scholar
    • Export Citation
  • FAO 2005 FAOSTAT Database, Rome, Italy: Food and Agriculture Organization of the United States. 24 Mar. 2014. <http://apps.fao.org/default.jsp>

  • FAO 2010 FaoStat: Agriculture Data. 24 Mar. 2014. <http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancor>

  • Fujii, K., Satomi, M., Morita, N., Motomura, T., Tanaka, T. & Kikuchi, S. 2003 Novosphingobium tardaugens sp. nov., an oestradiol degrading bacterium isolated from activated sludge of a sewage treatment plant in Tokyo Intl. J. Syst. Evol. Microbiol. 53 47 52

    • Search Google Scholar
    • Export Citation
  • Fulhage, C.D. & Pfost, D.L. 1994 Spreading poultry litter without lab analysis but with soil tests. Dept. of Agr., Univ. of Missouri Ext. WQ222

  • Gan, H.M., Hudson, A.O., Rahman, A.Y.A., Chan, K.G. & Savka, M.A. 2013 Comparative genomic analysis of six bacteria belonging to the genus Novosphingobium: Insights into marine adaptation, cell-cell signaling and bioremediation BMC Genomics 14 431

    • Search Google Scholar
    • Export Citation
  • Gaskell, M. & Smith, R. 2007 Nitrogen sources for organic vegetable crops HortTechnology 17 431 441

  • Gianfreda, L. 2015 Enzymes of importance to rhizosphere processes J. Soil Sci. Plant Nutr. 15 283 306

  • Gutierrez-Miceli, F.A., Santiago-Borraz, J., Montes Molina, J.A., Nafate, C.C., Abud-Archila, M., Oliva Llaven, M.A., Rincon-Rosales, R. & Dendooven, L. 2007 Vermicompost as a soil supplement to improve growth, yield and fruit quality of tomato (Lycopersicum esculentum) Bioresour. Technol. 98 2781 2786

    • Search Google Scholar
    • Export Citation
  • Hawes, M.C., Curlango-Rivera, G., Xiong, Z. & Kessler, J.O. 2012 Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA ‘trapping’ Plant Soil 355 1 16

    • Search Google Scholar
    • Export Citation
  • Herman, M.A.B., Nault, B.A. & Smart, C.D. 2008 Effects of plant growth promoting rhizobacteria on bell pepper production and green peach aphid infestation in New York Crop Prot. 27 996 1002

    • Search Google Scholar
    • Export Citation
  • Horne, P.A. 2008 Integrated pest management for crops and pastures. CSIRO, Melbourne, Australia

  • Janssen, P.H. 2006 Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes Appl. Environ. Microbiol. 72 1719 1728

    • Search Google Scholar
    • Export Citation
  • Jett, L.W. & Mulkey, W.A. 1996 Nitrogen fertilizer effects on growth and yield of sweetpotato HortScience 31 759 765

  • Kämpfer, P., Young, C.C., Busse, H.J., Lin, S.Y., Rekha, P.D., Arun, A.B., Chen, W.M., Shen, F.T. & Wu, Y.H. 2011 Novosphingobium soli sp. nov., isolated from soil Intl. J. Syst. Evol. Microbiol. 61 259 263

    • Search Google Scholar
    • Export Citation
  • Kämpfer, P., Martin, K., McInroy, J.A. & Glaeser, S.P. 2015 Novosphingobium gossypii sp. nov., isolated from Gossypium hirsutum Intl. J. Syst. Evol. Microbiol. 65 2831 2837

    • Search Google Scholar
    • Export Citation
  • Kennedy, A.C. 1995 Soil microbial diversity in agricultural systems, p. 249. In: R. Olson, F. Francis, and S. Kaffka (eds.). Exploring the role of diversity in sustainable agriculture. Amer. Soc. of Agr., Madison, WI

  • Khodadad, C.L., Zimmerman, A.R., Green, S.J., Uthandi, S. & Foster, J.S. 2011 Taxa-specific changes in soil microbial community composition induced by pyrogenic carbon amendments Soil Biol. Biochem. 43 385 392

    • Search Google Scholar
    • Export Citation
  • Klonsky, K. 2000 Forces impacting the production of organic foods Agr. Human Values 17 233 243

  • Lauber, C.L., Hamady, M., Knight, R. & Fierer, N. 2009 Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community composition at the continental scale Appl. Environ. Microbiol. 75 5111 5120

    • Search Google Scholar
    • Export Citation
  • Ledger, T., Zúñiga, A., Kraiser, T., Dasencich, P., Donoso, R., Pérez-Pantoja, D. & González, B. 2012 Aromatic compounds degradation plays a role in colonization of Arabidopsis thaliana and acacia cavern by Cupriavidus pinatubonensis JMP134 Antonie van Leeuwenhoek 101 713 723

    • Search Google Scholar
    • Export Citation
  • Leff, J.W. & Fierer, N. 2013 Bacterial communities associated with the surfaces of fresh fruits and vegetables PLoS One 8 e59310

  • Lin, S.Y., Hameed, A., Liu, Y.C., Hsu, Y.H., Lai, W.A., Huang, H.I. & Young, C.C. 2014 Novosphingobium arabidopsis sp. nov., a DDT-resistant bacterium isolated from the rhizosphere of Arabidopsis thaliana Intl. J. Syst. Evol. Microbiol. 64 594 598

    • Search Google Scholar
    • Export Citation
  • Li, R., Khafipour, E., Krause, D.O., Entz, M.H. & de Kievit, T.R. 2012 Pyrosequencing reveals the influence of organic and conventional farming systems on bacterial communities. PLoS One 7:e51897, doi: 10.1371/journal.pone.0051897

  • Liu, Z.P., Wang, B.J., Liu, Y.H. & Liu, S.J. 2005 Novosphingobium taihuense sp. nov., a novel aromatic-compound-degrading bacterium isolated from Taihu Lake, China Intl. J. Syst. Evol. Microbiol. 55 1229 1232

    • Search Google Scholar
    • Export Citation
  • Lynch, J.M. & Whipps, J.M. 1990 Substrate flow in the rhizosphere Plant Soil 129 1 10

  • Madigan, M.I., Cox, S.S. & Stegeman, R.A. 1984 Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae J. Bacteriol. 157 73 78

    • Search Google Scholar
    • Export Citation
  • Mikkelsen, R. & Hartz, T.K. 2008 Nitrogen sources for organic crop production Better Crops Plant Food 92 16 19

  • Moore-Kucera, J. & Dick, R.P. 2008 PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence Microb. Ecol. 55 500 511

    • Search Google Scholar
    • Export Citation
  • Mortley, D., Bonsi, C. & Amagloh, F.K. 2017 The influence of days after planting on root yield and quality of orange- and purple-fleshed sweetpotato (Ipomoea batatas (L.) Lam) cultivars assessed in the Northern Region, Ghana J. Ghana Sci. Assoc. 17 9 15

    • Search Google Scholar
    • Export Citation
  • Mortley, D.G. & Hill, W.A. 1990 Sweetpotato growth and nitrogen content following nitrogen application and inoculation with Azospirillum HortScience 25 758 759

    • Search Google Scholar
    • Export Citation
  • Ndiaye, E.L., Sandeno, J.M., McGrath, D. & Dick, R.P. 2000 Integrative biological indicators for detecting change in soil quality Amer. J. Altern. Agr. 15 26 36

    • Search Google Scholar
    • Export Citation
  • Neef, A., Witzenberger, R. & Kampfer, P. 1999 Detection of sphingomonads and in situ identification in activated sludge using 16S rRNA-targeted oligonucleotide probes J. Ind. Microbiol. Biotechnol. 23 261 267

    • Search Google Scholar
    • Export Citation
  • Parham, J.A. & Deng, S.P. 2000 Detection, quantification and characterization of beta-glucosaminidase activity in soil Soil Biol. Biochem. 32 1183 1190

    • Search Google Scholar
    • Export Citation
  • SAS Institute Inc 2009 The SAS system for windows, Version 9.2. SAS Institute Inc. Cary, NC

  • Shange, R.S., Ankumah, R.O., Ibekwe, A.M., Zabawa, R. & Dowd, S.E. 2012 Distinct soil bacterial communities revealed under a diversely managed agroecosystem PLoS One 7 e40338

    • Search Google Scholar
    • Export Citation
  • Sohn, J.H., Kwon, K.K., Kang, J.H., Jung, H.B. & Kim, S.J. 2004 Novosphingobium pentaromativorans sp. nov., a high-molecular-mass polycyclic aromatic hydrocarbon-degrading bacterium isolated from estuarine sediment Intl. J. Syst. Evol. Microbiol. 54 1483 1487

    • Search Google Scholar
    • Export Citation
  • Sugiyama, A., Vivanco, J.M., Jayanty, S.S. & Manter, D.K. 2010 Pyrosequencing assessment of soil microbial communities in organic and conventional potato farms Plant Dis. 94 1329 1335

    • Search Google Scholar
    • Export Citation
  • Sun, H.Y., Deng, S.P. & Raun, W.R. 2004 Bacterial community structure and diversity in a century-old manure-treated agroecosystem Appl. Environ. Ecol. 70 5868 5874

    • Search Google Scholar
    • Export Citation
  • Tabatabai, M.A. & Dick, W.A. 2002 Enzymes in soil: Research and developments in measuring activities, p. 539–565. In: R.G. Burns and R.P. Dick (eds.). Enzymes in the environment. Marcel Dekker, New York, NY

  • Treadwell, D.D., Creamer, N.G., Hoyt, G.D. & Schultheis, J.R. 2008 Nutrient management with cover crops and compost affects development and yield in organically managed sweetpotato systems HortScience 43 1423 1433

    • Search Google Scholar
    • Export Citation
  • Trotman, A.A., Hill, W.A., Mortley, D.G., David, P.P. & Loretan, P.A. 1993 Response of hydroponically grown sweetpotato to inoculation with Azospirillum HortScience 28 266

    • Search Google Scholar
    • Export Citation
  • Vessey, J.K. 2003 Plant growth promoting rhizobacteria as biofertilizers Plant Soil 255 571 586

  • Villordan, A., LaBonte, D., Firon, N. & Carey, E. 2013 Variation in nitrogen rate and local availability alter root architecture attributes at the onset of storage root initiation in ‘Beauregard’ sweetpotato HortScience 48 808 815

    • Search Google Scholar
    • Export Citation
  • Walkley, A. & Black, I.A. 1934 An examination of the Degtjareff method for determining organic carbon in soils: Effect of variations in digestion conditions and of inorganic soil constituents Soil Sci. 63 251 263

    • Search Google Scholar
    • Export Citation
  • Wang, Z., Zong, H., Zheng, H., Liu, G., Chen, L. & Xing, B. 2015 Reduced nitrification and abundance of ammonia-oxidizing bacteria in acidic soil amended with biochar Chemosphere 138 576 583

    • Search Google Scholar
    • Export Citation
  • Wen-yuan, H. 2007 Tight supply and strong demand may raise U.S. nitrogen fertilizer prices Amber Waves 5 7

  • Whitmore, A.P. 2007 Determination of the mineralization of nitrogen from composted chicken manure as affected by temperature Nutr. Cycl. Agroecosyst. 77 225 232

    • Search Google Scholar
    • Export Citation
  • Widmer, F., Rasche, F., Hartmann, M. & Fliessbach, A. 2006 Community structures and substrate utilization of bacteria in soils from organic and conventional farming systems of the DOK long-term field experiment Appl. Soil Ecol. 33 294 307

    • Search Google Scholar
    • Export Citation
  • Worthington, V. 2001 Nutritional quality of organic versus conventional fruits, vegetables, and grains J. Altern. Complement. Med. 7 161 173

  • Wu, Q., Knowles, R. & Niven, D.F. 1994 O2 regulation of denitrification in Flexibacter canadensis Can. J. Microbiol. 40 916 921

  • Zhang, H., Sekiguchi, Y., Hanada, S., Hugenholtz, P., Kim, H., Kamagata, Y. & Nakamura, K. 2003 Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating microorganism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov Intl. J. Syst. Evol. Microbiol. 53 1155 1163

    • Search Google Scholar
    • Export Citation

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Contributor Notes

Contribution of the George Washington Carver Agricultural Experiment Station, Tuskegee University. This research was supported by funds from U.S. Department of Agriculture/National Institute of Food and Agriculture Evans-Allen Grant No. ALX-FV. The authors extend deep gratitude toward all the staff at Tuskegee University George Washington Carver Agricultural Experiment Station.

Former graduate student. Current address: Department of Crop, Soil, and Environmental Sciences, College of Agriculture, Auburn University, Auburn, AL 36849.

Corresponding author. E-mail: dmortley@tuskegee.edu.

  • View in gallery

    Bacterial composition at the phylum level for each sample of sweetpotato rhizosphere. 0bh to 0tu = Control ‘TU Purple’, ‘J6/66’, ‘NCC-58’, ‘Whatley’; bl = poultry litter; fsh = Magabloom (fish hydrolysate); fert = NPK fertilizer all combined with the same four sweetpotato cultivars.

  • Ai, C., Liang, G., Sun, J., Wang, X. & Zhou, W. 2012 Response of ectracellular enzyme activities and microbial community in both the rhizosphere and bulk soil to long-term fertilization practices in a fluvo-aquic soil Geoderma 173–174 330 333

    • Search Google Scholar
    • Export Citation
  • Baker, B. 2005 Brief History of Organic Farming and the National Organic Program. In: Organic Farming Compliance Handbook. Organic Materials Review Institute, Eugene, OR

  • Balkwill, D.L., Drake, G.R., Reeves, R.H., Fredrickson, J.K., White, D.C., Ringelberg, D.B., Chandler, D.P., Romine, M.F., Kennedy, D.W. & Spadoni, C.M. 1997 Taxonomic study of aromatic degrading bacteria from deep-terrestrial-subsurface sediments and description of Sphingomonas aromaticivorans sp. nov., Sphingomonas subterranea sp. nov., and Sphingomonas stygia sp. nov Intl. J. Syst. Bacteriol. 47 191 201

    • Search Google Scholar
    • Export Citation
  • Bowen, G.D. & Rovira, A.D. 1976 Microbial colonization of plant roots Annu. Rev. Phytopathol. 114 121 144

  • Boyhan, G., Hicks, R.J., Torrance, R.L., Riner, C.M. & Hill, C.R. 2010 Evaluation of poultry litter and organic fertilizer rate and source for production of organic short-day onions HortTechnology 20 304 307

    • Search Google Scholar
    • Export Citation
  • Bruinsma, M., Kowalchuk, G.A. & Van Veen, J.A. 2003 Effects of genetically modified plants on microbial communities and processes in soil Biol. Fertil. Soils 37 329 337

    • Search Google Scholar
    • Export Citation
  • Burns, R.G. 1983 Extracellular enzyme-substrate interactions in soil, p. 249. In: J.H. Slater, R. Whittenbury, and J.W.T. Wimpenny (eds.). Microbes in their natural environment. Cambridge University Press, Cambridge, UK

  • CSPI 1992 Sweetpotato nutrition. Washington D.C. USA. 24 Mar. 2018. <http://www.foodreference.com/html/sweet-pot-nutrition.html>

  • Chang, W.H., Huang, Y.F., Yeh, T.S. & Liu, J.F. 2010 Effect of purple sweetpotato leaves consumption on exercise-induced oxidative stress, and IL-6 and HSP72 levels J. Appl. Physiol. 109 1710 1715

    • Search Google Scholar
    • Export Citation
  • Chaudhry, V., Rehman, A., Mishra, A., Chauhan, P.S. & Nautiyal, C.S. 2012 Changes in bacterial community structure of agricultural land due to long-term organic and chemical amendments Microb. Ecol. 64 450 460

    • Search Google Scholar
    • Export Citation
  • Choi, J.H., Choi, C.Y., Lee, K.J., Hwang, Y.P., Chung, Y.C. & Jeong, H.G. 2009 Hepatoprotective effects of an anthocyanin fraction from purple-fleshed sweet potato against acetaminophen-induced liver damage in mice J. Med. Food 12 320 326

    • Search Google Scholar
    • Export Citation
  • Coleman, D.C., Crossley, D.A. & Hendrix, P.F. 2004 Fundamentals of soil ecology. 2nd ed. Elsevier Inc., Burlington, VT

  • Collado, L.S., Mabesa, R.C. & Corke, H. 1999 Genetic variation in the physical properties of sweet potato starch J. Agr. Food Chem. 47 4195 4201

  • Crump, E.M., Perry, M.B., Gale, S., Crawford, E. & Kay, W.W. 2003 Lipopolysaccharide O-antigen antibody-based detection of the fish pathogen Flavobacterium psychrophilum J. Mol. Microbiol. Biotechnol. 6 182 190

    • Search Google Scholar
    • Export Citation
  • Delate, K., Duffy, M., Chase, C., Holste, A., Friedrich, H. & Wantate, N. 2003 An economic comparison of organic and conventional grain crops in a long-term agroecological research (LTAR) site in Iowa Amer. J. Altern. Agr. 18 59 69

    • Search Google Scholar
    • Export Citation
  • Edmeades, D.C. 2003 The long-term effects of manures and fertilisers on soil productivity and quality: A review Nutr. Cycl. Agroecosyst. 66 165 180

    • Search Google Scholar
    • Export Citation
  • Eivazi, F. & Tabatabai, M.A. 1977 Phosphatases in soils Soil Biol. Biochem. 9 167 172

  • Ekenler, M. & Tabatabai, M.A. 2003 Tillage and residue management effects on beta-glucosaminidase activity in soils Soil Biol. Biochem. 35 871 874

  • Failla, M.L., Thakkar, S.K. & Kim, J.Y. 2009 In vitro bioaccessibility of beta-carotene in orange fleshed sweet potato (Ipomoea batatas Lam.) J. Agr. Food Chem. 57 10922 10927

    • Search Google Scholar
    • Export Citation
  • FAO 2005 FAOSTAT Database, Rome, Italy: Food and Agriculture Organization of the United States. 24 Mar. 2014. <http://apps.fao.org/default.jsp>

  • FAO 2010 FaoStat: Agriculture Data. 24 Mar. 2014. <http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567#ancor>

  • Fujii, K., Satomi, M., Morita, N., Motomura, T., Tanaka, T. & Kikuchi, S. 2003 Novosphingobium tardaugens sp. nov., an oestradiol degrading bacterium isolated from activated sludge of a sewage treatment plant in Tokyo Intl. J. Syst. Evol. Microbiol. 53 47 52

    • Search Google Scholar
    • Export Citation
  • Fulhage, C.D. & Pfost, D.L. 1994 Spreading poultry litter without lab analysis but with soil tests. Dept. of Agr., Univ. of Missouri Ext. WQ222

  • Gan, H.M., Hudson, A.O., Rahman, A.Y.A., Chan, K.G. & Savka, M.A. 2013 Comparative genomic analysis of six bacteria belonging to the genus Novosphingobium: Insights into marine adaptation, cell-cell signaling and bioremediation BMC Genomics 14 431

    • Search Google Scholar
    • Export Citation
  • Gaskell, M. & Smith, R. 2007 Nitrogen sources for organic vegetable crops HortTechnology 17 431 441

  • Gianfreda, L. 2015 Enzymes of importance to rhizosphere processes J. Soil Sci. Plant Nutr. 15 283 306

  • Gutierrez-Miceli, F.A., Santiago-Borraz, J., Montes Molina, J.A., Nafate, C.C., Abud-Archila, M., Oliva Llaven, M.A., Rincon-Rosales, R. & Dendooven, L. 2007 Vermicompost as a soil supplement to improve growth, yield and fruit quality of tomato (Lycopersicum esculentum) Bioresour. Technol. 98 2781 2786

    • Search Google Scholar
    • Export Citation
  • Hawes, M.C., Curlango-Rivera, G., Xiong, Z. & Kessler, J.O. 2012 Roles of root border cells in plant defense and regulation of rhizosphere microbial populations by extracellular DNA ‘trapping’ Plant Soil 355 1 16

    • Search Google Scholar
    • Export Citation
  • Herman, M.A.B., Nault, B.A. & Smart, C.D. 2008 Effects of plant growth promoting rhizobacteria on bell pepper production and green peach aphid infestation in New York Crop Prot. 27 996 1002

    • Search Google Scholar
    • Export Citation
  • Horne, P.A. 2008 Integrated pest management for crops and pastures. CSIRO, Melbourne, Australia

  • Janssen, P.H. 2006 Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes Appl. Environ. Microbiol. 72 1719 1728

    • Search Google Scholar
    • Export Citation
  • Jett, L.W. & Mulkey, W.A. 1996 Nitrogen fertilizer effects on growth and yield of sweetpotato HortScience 31 759 765

  • Kämpfer, P., Young, C.C., Busse, H.J., Lin, S.Y., Rekha, P.D., Arun, A.B., Chen, W.M., Shen, F.T. & Wu, Y.H. 2011 Novosphingobium soli sp. nov., isolated from soil Intl. J. Syst. Evol. Microbiol. 61 259 263

    • Search Google Scholar
    • Export Citation
  • Kämpfer, P., Martin, K., McInroy, J.A. & Glaeser, S.P. 2015 Novosphingobium gossypii sp. nov., isolated from Gossypium hirsutum Intl. J. Syst. Evol. Microbiol. 65 2831 2837

    • Search Google Scholar
    • Export Citation
  • Kennedy, A.C. 1995 Soil microbial diversity in agricultural systems, p. 249. In: R. Olson, F. Francis, and S. Kaffka (eds.). Exploring the role of diversity in sustainable agriculture. Amer. Soc. of Agr., Madison, WI

  • Khodadad, C.L., Zimmerman, A.R., Green, S.J., Uthandi, S. & Foster, J.S. 2011 Taxa-specific changes in soil microbial community composition induced by pyrogenic carbon amendments Soil Biol. Biochem. 43 385 392

    • Search Google Scholar
    • Export Citation
  • Klonsky, K. 2000 Forces impacting the production of organic foods Agr. Human Values 17 233 243

  • Lauber, C.L., Hamady, M., Knight, R. & Fierer, N. 2009 Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community composition at the continental scale Appl. Environ. Microbiol. 75 5111 5120

    • Search Google Scholar
    • Export Citation
  • Ledger, T., Zúñiga, A., Kraiser, T., Dasencich, P., Donoso, R., Pérez-Pantoja, D. & González, B. 2012 Aromatic compounds degradation plays a role in colonization of Arabidopsis thaliana and acacia cavern by Cupriavidus pinatubonensis JMP134 Antonie van Leeuwenhoek 101 713 723

    • Search Google Scholar
    • Export Citation
  • Leff, J.W. & Fierer, N. 2013 Bacterial communities associated with the surfaces of fresh fruits and vegetables PLoS One 8 e59310

  • Lin, S.Y., Hameed, A., Liu, Y.C., Hsu, Y.H., Lai, W.A., Huang, H.I. & Young, C.C. 2014 Novosphingobium arabidopsis sp. nov., a DDT-resistant bacterium isolated from the rhizosphere of Arabidopsis thaliana Intl. J. Syst. Evol. Microbiol. 64 594 598

    • Search Google Scholar
    • Export Citation
  • Li, R., Khafipour, E., Krause, D.O., Entz, M.H. & de Kievit, T.R. 2012 Pyrosequencing reveals the influence of organic and conventional farming systems on bacterial communities. PLoS One 7:e51897, doi: 10.1371/journal.pone.0051897

  • Liu, Z.P., Wang, B.J., Liu, Y.H. & Liu, S.J. 2005 Novosphingobium taihuense sp. nov., a novel aromatic-compound-degrading bacterium isolated from Taihu Lake, China Intl. J. Syst. Evol. Microbiol. 55 1229 1232

    • Search Google Scholar
    • Export Citation
  • Lynch, J.M. & Whipps, J.M. 1990 Substrate flow in the rhizosphere Plant Soil 129 1 10

  • Madigan, M.I., Cox, S.S. & Stegeman, R.A. 1984 Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae J. Bacteriol. 157 73 78

    • Search Google Scholar
    • Export Citation
  • Mikkelsen, R. & Hartz, T.K. 2008 Nitrogen sources for organic crop production Better Crops Plant Food 92 16 19

  • Moore-Kucera, J. & Dick, R.P. 2008 PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence Microb. Ecol. 55 500 511

    • Search Google Scholar
    • Export Citation
  • Mortley, D., Bonsi, C. & Amagloh, F.K. 2017 The influence of days after planting on root yield and quality of orange- and purple-fleshed sweetpotato (Ipomoea batatas (L.) Lam) cultivars assessed in the Northern Region, Ghana J. Ghana Sci. Assoc. 17 9 15

    • Search Google Scholar
    • Export Citation
  • Mortley, D.G. & Hill, W.A. 1990 Sweetpotato growth and nitrogen content following nitrogen application and inoculation with Azospirillum HortScience 25 758 759

    • Search Google Scholar
    • Export Citation
  • Ndiaye, E.L., Sandeno, J.M., McGrath, D. & Dick, R.P. 2000 Integrative biological indicators for detecting change in soil quality Amer. J. Altern. Agr. 15 26 36

    • Search Google Scholar
    • Export Citation
  • Neef, A., Witzenberger, R. & Kampfer, P. 1999 Detection of sphingomonads and in situ identification in activated sludge using 16S rRNA-targeted oligonucleotide probes J. Ind. Microbiol. Biotechnol. 23 261 267

    • Search Google Scholar
    • Export Citation
  • Parham, J.A. & Deng, S.P. 2000 Detection, quantification and characterization of beta-glucosaminidase activity in soil Soil Biol. Biochem. 32 1183 1190

    • Search Google Scholar
    • Export Citation
  • SAS Institute Inc 2009 The SAS system for windows, Version 9.2. SAS Institute Inc. Cary, NC

  • Shange, R.S., Ankumah, R.O., Ibekwe, A.M., Zabawa, R. & Dowd, S.E. 2012 Distinct soil bacterial communities revealed under a diversely managed agroecosystem PLoS One 7 e40338

    • Search Google Scholar
    • Export Citation
  • Sohn, J.H., Kwon, K.K., Kang, J.H., Jung, H.B. & Kim, S.J. 2004 Novosphingobium pentaromativorans sp. nov., a high-molecular-mass polycyclic aromatic hydrocarbon-degrading bacterium isolated from estuarine sediment Intl. J. Syst. Evol. Microbiol. 54 1483 1487

    • Search Google Scholar
    • Export Citation
  • Sugiyama, A., Vivanco, J.M., Jayanty, S.S. & Manter, D.K. 2010 Pyrosequencing assessment of soil microbial communities in organic and conventional potato farms Plant Dis. 94 1329 1335

    • Search Google Scholar
    • Export Citation
  • Sun, H.Y., Deng, S.P. & Raun, W.R. 2004 Bacterial community structure and diversity in a century-old manure-treated agroecosystem Appl. Environ. Ecol. 70 5868 5874

    • Search Google Scholar
    • Export Citation
  • Tabatabai, M.A. & Dick, W.A. 2002 Enzymes in soil: Research and developments in measuring activities, p. 539–565. In: R.G. Burns and R.P. Dick (eds.). Enzymes in the environment. Marcel Dekker, New York, NY

  • Treadwell, D.D., Creamer, N.G., Hoyt, G.D. & Schultheis, J.R. 2008 Nutrient management with cover crops and compost affects development and yield in organically managed sweetpotato systems HortScience 43 1423 1433

    • Search Google Scholar
    • Export Citation
  • Trotman, A.A., Hill, W.A., Mortley, D.G., David, P.P. & Loretan, P.A. 1993 Response of hydroponically grown sweetpotato to inoculation with Azospirillum HortScience 28 266

    • Search Google Scholar
    • Export Citation
  • Vessey, J.K. 2003 Plant growth promoting rhizobacteria as biofertilizers Plant Soil 255 571 586

  • Villordan, A., LaBonte, D., Firon, N. & Carey, E. 2013 Variation in nitrogen rate and local availability alter root architecture attributes at the onset of storage root initiation in ‘Beauregard’ sweetpotato HortScience 48 808 815

    • Search Google Scholar
    • Export Citation
  • Walkley, A. & Black, I.A. 1934 An examination of the Degtjareff method for determining organic carbon in soils: Effect of variations in digestion conditions and of inorganic soil constituents Soil Sci. 63 251 263

    • Search Google Scholar
    • Export Citation
  • Wang, Z., Zong, H., Zheng, H., Liu, G., Chen, L. & Xing, B. 2015 Reduced nitrification and abundance of ammonia-oxidizing bacteria in acidic soil amended with biochar Chemosphere 138 576 583

    • Search Google Scholar
    • Export Citation
  • Wen-yuan, H. 2007 Tight supply and strong demand may raise U.S. nitrogen fertilizer prices Amber Waves 5 7

  • Whitmore, A.P. 2007 Determination of the mineralization of nitrogen from composted chicken manure as affected by temperature Nutr. Cycl. Agroecosyst. 77 225 232

    • Search Google Scholar
    • Export Citation
  • Widmer, F., Rasche, F., Hartmann, M. & Fliessbach, A. 2006 Community structures and substrate utilization of bacteria in soils from organic and conventional farming systems of the DOK long-term field experiment Appl. Soil Ecol. 33 294 307

    • Search Google Scholar
    • Export Citation
  • Worthington, V. 2001 Nutritional quality of organic versus conventional fruits, vegetables, and grains J. Altern. Complement. Med. 7 161 173

  • Wu, Q., Knowles, R. & Niven, D.F. 1994 O2 regulation of denitrification in Flexibacter canadensis Can. J. Microbiol. 40 916 921

  • Zhang, H., Sekiguchi, Y., Hanada, S., Hugenholtz, P., Kim, H., Kamagata, Y. & Nakamura, K. 2003 Gemmatimonas aurantiaca gen. nov., sp. nov., a Gram-negative, aerobic, polyphosphate-accumulating microorganism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov Intl. J. Syst. Evol. Microbiol. 53 1155 1163

    • Search Google Scholar
    • Export Citation
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