Lignin is a plant cell wall constituent that acts as a protective matrix and limits the availability of readily biodegradable plant materials, such as cellulose and hemi-celluloses, for microbial degradation (Ledeboer and Skogly, 1967). Lignin is formed in plants by oxidative coupling of monolignols of three primary hydroxycinnamyl alcohols: p-coumaryl, coniferyl, and sinapyl alcohols (Wong, 2009). Lignin is extremely recalcitrant to degradation due to its complex structure without a regular pattern, which is derived from random oxidative coupling of lignin monomers and cross-linking of polymers via radical mechanisms; this process is known as lignification (Ledeboer and Skogly, 1967). A lignin macromolecule contains monolignols randomly bonded by C-O-C and C-C linkages including β-O-4, β-5, β-β, 5-5, 4-O-5, and β-1 bonds (Alder, 1977; Del Rio et al., 2007; Ralph et al., 2004). Several models of the lignin molecular structure have been proposed, but these models do not imply any particular sequence of monomeric units in the lignin macromolecule (Chen and Sarkanen, 2003; Davin and Lewis, 2003). Other researchers have indicated a homogeneous structure of lignin based on studies suggesting lignin formation by repetitive units (Banoub and Delmas, 2003).
The formation of a thatch-mat layer at home lawn and recreational turfgrass sites, especially golf greens, is accelerated when organic matter production exceeds the degradation rate (Beard, 1973). Thatch, a layer of highly organic matter that accumulates between the soil and green turfgrass, consists of dead and living stolon, rhizome, root, crown, leaf sheath, and blade tissues (Engel, 1954; Roberts and Bredakis, 1960). A mat layer is generally below the thatch layer, where soil or sand is intermingled with thatch as a result of earthworm activity or cultural practices, such as core aeration and topdressing (McCarty, 2005). A thatch layer is often desirable to increase resilience and wear tolerance of the turfgrass surface, reduce surface hardness, and moderate soil temperature extremes (Beard, 1973). However, an excessive thatch or mat layer is undesirable in turfgrass because it leads to decreased saturated hydraulic conductivity (SHC), decreased movement of oxygen through the thatch or mat zone, low oxygen levels within the thatch/mat layer during wet periods, and increased water retention (Carrow, 2003; Hartwiger, 2004; McCarty et al., 2007).
Cultural or mechanical control practices of core aeration, vertical mowing, grooming, and topdressing are often effective for reducing thatch, but they are known to adversely impact turf quality (Landreth et al., 2008; McCarty et al., 2007). Additionally, these practices have intensive requirements for labor, equipment, and energy (Barton et al., 2009; Landreth et al., 2008; McCarty et al., 2007), and they have shown contrasting results regarding reducing the organic matter content in the thatch layer (Barton et al., 2009; Carrow et al., 1987; Dunn et al., 1981; McCarty et al., 2005; McWhirter and Ward, 1976; Weston and Dunn, 1985; White and Dickens, 1984). Nondestructive biological and chemical attempts to enhance organic matter degradation in the thatch layer have included the usage of glucose, cellulase solutions (Ledeboer and Skogly, 1967), and commercial products containing mixtures of amino acids, microbial inocula, and fertilizers. These products target the degradation of cellulosic and hemi-cellulosic sugars in thatch biomass by improving conditions for microbial populations. However, the efficacy of these products have been inconsistent for reducing thatch in turfgrass (Lancaster et al., 1977; McCarty et al., 2005; Murdoch and Barr, 1976)
The rate of microbial decomposition is partially dependent on the lignin content of organic matter. Lignin degradation can act as the rate-limiting step in organic matter decomposition (Taylor et al., 1989). Sinsabaugh et al. (1993) conducted a plant litter decomposition study and reported a close relationship between lignocellulose-degrading enzymes and plant litter mass loss. Certain white-rot fungi are responsible for the natural degradation of lignin by producing extracellular lignolytic enzymes, thus exposing cellulosic materials to further bacterial degradation in the environment (Blanchette, 1984; Kirk et al., 1975, 1976; Mester et al., 2004; Otjen and Blanchette, 1987). Lignolytic enzymes such as tyrosinoses, catechol oxidases, laccase, catechol dioxygenases, and monophenol monooxygenase that use oxygen as an electron acceptor to oxidize phenolic compounds are likely present in environmental samples and provide estimates of the sum of activity from all or some combinations of these enzymes. Therefore, in most published work, the collective activity of these enzymes is referred to as phenol oxidase, which represents the activity of enzymes that use oxygen and oxidize phenols. Phenol oxidase activity in the top 7.5 cm of soil samples of turfgrass systems has been reported to range from 0.7 to 2.8 mmol/kg soil/h (Yao et al., 2009, 2011).
Weight loss of bermudagrass pellets, st. augustinegrass [Stenotaphrum secundatum (Walt.) Kuntze], and zoysiagrass (Zoysia japonica Stued., ‘Meyer’) stolons were observed when inoculated with different wood-decaying fungi under controlled greenhouse and laboratory conditions (Martin and Dale, 1980). In similar controlled studies, researchers have reported reductions in cellulose content and total oxidizable organic matter of bermudagrass (Cynodon dactylon L.) and centipedegrass (Eremochloa ophiuroides) after inoculation with wood-decaying fungi (Sartain and Volk, 1984). However, field inoculation experiments involving bermudagrass showed no thatch degradation (Martin and Dale, 1980). Microbial inoculation under field conditions may be ineffective because it is difficult to maintain specific microbial activity for longer periods under turfgrass management systems (Yao et al., 2009, 2011).
Under greenhouse conditions, decreases in the rate of thatch layer build-up and accumulations of total organic matter in the top 2.5 cm of creeping bentgrass were reported in response to the direct application of laccase, an extracellular lignolytic enzyme produced from white-rot fungi Trametes versicolor (Sidhu et al., 2012). However, a net accumulation of organic matter in the thatch layer treated with laccase was observed over time with all treatments (Sidhu et al., 2012). A biweekly application of laccase enzymes on the thatch layer of dead creeping bentgrass verified the effectiveness of laccase for facilitating organic matter decomposition and the loss of the total sugar content of the thatch biomass. These results suggested that laccase application exposed cellulosic and hemi-cellulosic sugars to microbial degradation by opening the biomass structure (Sidhu et al., 2013a). Field studies conducted using creeping bentgrass, ultra-dwarf bermudagrass, and zoysiagrass verified the effectiveness of laccase for thatch management on different turfgrass species (Sidhu et al., 2013b, 2014). In other experiments, creeping bentgrass treated biweekly with laccase, core aeration, and sand topdressing had significant reductions in thatch accumulation (Sidhu et al., 2014). In previous studies, organic matter degradation in response to enzyme treatment was determined during and at the end of the application period (Sidhu et al., 2012, 2013a, 2013b, 2014).
The fate of naturally occurring laccase enzymes depends on the interaction with soil, which is composed of mineral constituents and organic matter. These soil constituents can adsorb extracellular enzymes and provide surfaces for enzymatic reactions. Adsorption of enzymes to soil constituents can immobilize laccase enzymes (Giaveno et al., 2010), change their efficacy (Ahn et al., 2007; Gianfreda and Bollag, 1994; Zimmerman et al., 2004), and change their stability and denaturation (Rao et al., 2000; Yan et al., 2010). Gianfreda and Bollag (1994) observed that montmorillonite and Kolinite adsorbed 71% and 64% of laccase, respectively. However, compared with free enzymes, the kinetic parameters of laccase were improved when immobilized on montmorillonite. Wu et al. (2014) also observed similar results when laccase was adsorbed on iron and aluminum minerals for 18 h. However, the long-term residual impacts of laccase under field conditions, particularly the presence of thatch and mat layers, requires investigation. The current study was designed to expand the results of previous studies by investigating the residual effects of laccase application on organic matter degradation. Knowledge of any residual effects would lead to turf management and economic implications. Therefore, the major objectives of this study were to determine the residual effects of laccase application on physical and chemical properties of the thatch layer of creeping bentgrass and to compare the residual effects of laccase with and without repeated applications.
AhnM.Y.ZimmermanA.R.MartinezC.E.ArchibaldD.D.BollagJ.M.DecemberJ.2007Characteristics of Trametes villosa laccase adsorbed on aluminum hydroxideEnzyme Microb. Technol.41141148
BanoubJ.H.DelmasM.2003Structural elucidation of wheat straw lignin polymer by atmospheric pressure chemical ionization tandem mass spectrometry and matrix-assisted laser desorption/ionization time-of-flight mass spectrometryJ. Mass Spectrom.38900903
BartonL.WanG.G.Y.BuckR.P.ColmerT.D.2009Effectiveness of cultural thatch-mat controls for young and mature kikuyu turfgrassAgron. J.1016774
BeardJ.B.1973Turfgrass: Science and culture. Prentice Hall Inc. Englewood Cliffs NJ
CanawayP.M.IsaacS.P.BennettR.A.1986The effects of mechanical treatments on the water infiltration rate of a sand playing surface for association footballJ. Sports Turf Res. Inst.626773
CarrowR.N.JohnsonB.J.BurnsR.E.1987Thatch and quality of Tifway bermudagrass turf in relation to fertility and cultivationAgron. J.79524530
DavinL.B.LewisN.G.2003A historical perspective on lignin biosynthesis: Monolignol, allylphenol and hydroxycinnamic acid coupling and downstream metabolismPhytochem. Rev.2257288
EngelR.E.AlderferR.B.1967The effect of cultivation, top-dressing, lime, N, and wetting agent on thatch development on 1/4-inch bentgrass over a 10-year periodN.J. Agric. Exp. Stn. Bull.8183245
GiavenoC.CeliL.RichardsonA.E.SimpsonR.J.BarberisE.2010Interaction of phytases with minerals and availability of substrate affect the hydrolysis of inositol phosphatesSoil Biol. Biochem.42491498
HartwigerC.2004The importance of organic matter dynamics: How research uncovered the primary cause of secondary problemsUSGA Green Sect. Rec.42911
KirkT.K.ConnorsW.J.BleamR.D.JeikusG.1976Requirements for a growth substrate during lignin decomposition by two wood-rotting fungiAppl. Environ. Microbiol.32192194
KirkT.K.ConnorsW.J.BleamR.D.HackettW.F.JeikusJ.G.1975Preparation and microbial decomposition of synthetic [14C] ligninsProc. Natl. Acad. Sci. USA7225152519
LandrethJ.KarcherD.RichardsonM.2008Cultivating to manage organic matter in sand based putting greens: University of Arkansas researchers provide important insight for managing organic buildup on putting greensUSGA Turfgrass Environ. Res. Online461619
McCartyL.B.2005Best golf course management practices. 2nd ed. Prentice Hall Inc. Upper Saddle River NJ
McCartyL.B.GreggM.F.TolerJ.E.CamberatoJ.J.HillH.S.2005Minimizing thatch and mat development in a newly seeded creeping bentgrass golf greenCrop Sci.4515291535
MesterT.VarelaE.TienM.2004Wood degradation by brown-rot and white-rot fungi. The Mycota II: Genetics and biotechnology. 2nd edition. Springer-Verlag Berlin Heidelberg
MunozC.GuillenF.MartinezA.T.MartinezM.J.1997Laccase isozymes of Pleurotus eryngii: Characterization, catalytic properties, and participation in activation of molecular oxygen and Mn2+ oxidationAppl. Environ. Microbiol.6321662174
MurdochC.L.BarrJ.P.1976Ineffectiveness of commercial microorganism inoculums in breaking down thatch in common bermudagrass in HawaiiHortScience11488489
MurrayJ.J.JuskaF.V.1977Effect of management practices on thatch accumulation, turf quality, and leaf spot damage in common Kentucky bluegrassAgron. J.69365369
National Renewable Energy Laboratory2008Determination of structural carbohydrates and lignin in biomass. NREL Golden CO. 7 June 2019. <http://www.nrel.gov/biomass/pdfs/42618.pdf>
ParkJ.W.DecJ.KimJ.E.BollagJ.M.1999Effect of humic constituents on the transformation of chlorinated phenols and anilines in the presence of oxidoreductive enzymes or birnessiteEnviron. Sci. Technol.3320282034
RalphJ.BunzelM.MaritaJ.M.HatfieldR.D.LuF.KimH.SchatzP.F.GrabberJ.H.SteinhartH.2004Peroxidase dependent cross linking reactions of p-hydroxicinnamates in plant cell wallsPhytochem. Rev.37996
RaoM.A.ViolanteA.GianfredaL.2000Interaction of acid phosphatase with clays, organic molecules, and organo-mineral complexes: Kinetics and stabilitySoil Biol. Biochem.3210071014
SartainJ.B.VolkB.G.1984Influence of selected white-rot fungi and topdressings on the composition of thatch components of four turfgrassesAgron. J.76359362
SAS Institute Inc1994The SAS system for windows. Release 9.2. SAS Inst. Cary NC
SidhuS.S.HuangQ.CarrowR.N.RaymerP.L.2013aLaccase mediated changes in physical and chemical composition properties of thatch layer in creeping bentgrass (Agrostis stolonifera L.)Soil Biol. Biochem.644856
SidhuS.S.HuangQ.CarrowR.N.RaymerP.L.2013bEfficacy of fungal laccase to facilitate biodethatching in bermudagrass and zoysiagrassAgron. J.10512471252
SidhuS.S.HuangQ.CarrowR.N.RaymerP.L.2014Optimizing laccase application on creeping bentgrass (Agrostis stolonifera L.) to facilitate biodethatchingCrop Sci.5418041815
SinsabaughR.L.AntibusR.K.LinkinsA.E.McclaughertyC.A.RayburnL.RepertD.WeilandT.1993Wood decomposition - nitrogen and phosphorus dynamics in relation to extracellular enzyme-activityEcology7415861593
StoilovaI.KrastanovA.StanchevV.2010Properties of crude laccase from Trametes versicolor produced by solid-substrate fermentationAdv. Biosci. Biotechnol.1208215
TaylorB.R.ParkinsonD.ParsonsW.F.J.1989Nitrogen and lignin content as predictors of litter decay rates: A microcosm testEcology7097104
U.S. Golf Association Green Section Staff1973Refining the green section specifications for putting green constructionUSGA Green Sect. Rec.1118
WestonJ.B.DunnJ.H.1985Thatch and quality of Meyer zoysia in response to mechanical cultivation and nitrogen fertilization p. 449–458. In: F. Lemaire (ed.). Proc. 5th Intl. Turfgrass Res. Conf. Avignon France. 1–5 July 1985. Institut National de la Recherche Agronomique Paris France
WuY.JiangY.JiaoJ.LiuM.HuF.2014Adsorption of Trametes versicolor laccase to soil iron and aluminum minerals: Enzyme activity, kinetics, and stability studiesColloids Surf. B Biointerfaces114342348
YanJ.PanG.DingC.QuanG.2010Kinetic and thermodynamic parameters of β-glucosidase immobilized on various colloidal particles from a paddy soilColloids Surf. B Biointerfaces79298303
YaoH.BowmanD.SheiW.2011Seasonal variations of soil microbial biomass and activity in warm- and cool-season turfgrass systemsSoil Biol. Biochem.4315361543
YaoH.BowmanD.RuftyT.SheiW.2009Interactions between N fertilizations, grass clipping addition and pH in turf ecosystems: Implications for soil enzyme activities and organic matter decompositionSoil Biol. Biochem.4114251432
ZimmermanA.R.ChoroverJ.GoyneK.W.BrantleyS.L.2004Protection of mesopore-adsorbed organic matter from enzymatic degradationEnviron. Sci. Technol.3845424548