Bacteria from the endosphere and rhizosphere of Quercus spp. use mainly cell wall-associated enzymes to decompose organic matter

. 2019 ; 14 (3) : e0214422. [epub] 20190325

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30908541

Due to the ability of soil bacteria to solubilize minerals, fix N2 and mobilize nutrients entrapped in the organic matter, their role in nutrient turnover and plant fitness is of high relevance in forest ecosystems. Although several authors have already studied the organic matter decomposing enzymes produced by soil and plant root-interacting bacteria, most of the works did not account for the activity of cell wall-attached enzymes. Therefore, the enzyme deployment strategy of three bacterial collections (genera Luteibacter, Pseudomonas and Arthrobacter) associated with Quercus spp. roots was investigated by exploring both cell-bound and freely-released hydrolytic enzymes. We also studied the potential of these bacterial collections to produce enzymes involved in the transformation of plant and fungal biomass. Remarkably, the cell-associated enzymes accounted for the vast majority of the total activity detected among Luteibacter strains, suggesting that they could have developed a strategy to maintain the decomposition products in their vicinity, and therefore to reduce the diffusional losses of the products. The spectrum of the enzymes synthesized and the titres of activity were diverse among the three bacterial genera. While cellulolytic and hemicellulolytic enzymes were rather common among Luteibacter and Pseudomonas strains and less detected in Arthrobacter collection, the activity of lipase was widespread among all the tested strains. Our results indicate that a large fraction of the extracellular enzymatic activity is due to cell wall-attached enzymes for some bacteria, and that Quercus spp. root bacteria could contribute at different levels to carbon (C), phosphorus (P) and nitrogen (N) cycles.

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Baldrian P. Forest microbiome: Diversity, complexity and dynamics. FEMS Microbiol Rev. 2017;41: 109–130. 10.1093/femsre/fuw040 PubMed DOI

Crowther TW, Glick HB, Covey KR, Bettigole C, Maynard DS, Thomas SM, et al. Mapping tree density at global scale. Nature. 2015;525: 201–205. 10.1038/nature14967 PubMed DOI

Janssens IA, Freibauer A, Ciais P, Smith P, Nabuurs GJ, Folberth G, et al. Europe's terrestrial biosphere absorbs 7 to 12% of European anthropogenic CO2 emissions. Science. 2003;300: 1538–1542. 10.1126/science.1083592 PubMed DOI

Lladó S, López-Mondéjar R, Baldrian P. Forest soil Bacteria: diversity, involvement in ecosystem processes, and response to global change. Microbiol Mol Biol Rev. 2017;8: e00063–16. 10.1128/MMBR.00063-16 PubMed DOI PMC

Voříšková J, Brabcová V, Cajthaml T, Baldrian P. Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol. 2014;201: 269–278. 10.1111/nph.12481 PubMed DOI

Sterkenburg E, Bahr A, Brandstrom Durling M, Clemmensen KE, Lindahl BD. Changes in fungal communities along a boreal forest soil fertility gradient. New Phytol. 2015;207: 1145–1158. 10.1111/nph.13426 PubMed DOI

Boer W, Folman LB, Summerbell RC, Boddy L. Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev. 2005;29: 795–811. 10.1016/j.femsre.2004.11.005 PubMed DOI

Eichorst SA, Kuske CR. Identification of cellulose-responsive bacterial and fungal communities in geographically and edaphically different soils by using stable isotope probing. Appl Environ Microbiol. 2012;78: 2316–2327. 10.1128/AEM.07313-11 PubMed DOI PMC

Štursová M, Žifčáková L, Leigh MB, Burgess R, Baldrian P. Cellulose utilization in forest litter and soil: identification of bacterial and fungal decomposers. FEMS Microbiol Ecol. 2012;80: 735–746. 10.1111/j.1574-6941.2012.01343.x PubMed DOI

Lladó S, Žifčáková L, Větrovský T, Eichlerová I, Baldrian P. Functional screening of abundant bacteria from acidic forest soil indicates the metabolic potential of Acidobacteria subdivision 1 for polysaccharide decomposition. Biol Fertil Soils. 2016;52: 251–260. 10.1007/s00374-015-1072-6 DOI

López-Mondéjar R, Zühlke D, Becher D, Riedel K, Baldrian P. Cellulose and hemicellulose decomposition by forest soil bacteria proceeds by the action of structurally variable enzymatic systems. Sci Rep. 2016;6: 25279 10.1038/srep25279 PubMed DOI PMC

Nakano H, Okamoto K, Yatake T, Kiso T, Kitahata S. Purification and characterization of a novel beta-glucosidase from Clavibacter michiganense that hydrolyzes glucosyl ester linkage in steviol glycosides. J Ferment Bioeng 1998;85: 162–168. 10.1016/S0922-338X(97)86761-X DOI

Yin LJ, Huang PS, Lin HH. Isolation of Cellulase-Producing Bacteria and characterization of the Cellulase from the isolated bacterium Cellulomonas sp YJ5. J Agric Food Chem 2010;58: 9833–9837. 10.1021/jf1019104 PubMed DOI

Song JM, Wei DZ. Production and characterization of cellulases and xylanases of Cellulosimicrobium cellulans grown in pretreated and extracted bagasse and minimal nutrient medium M9. Biomass Bioenergy 2010;34: 1930–1934.

Fan HX, Miao LL, Liu Y, Liu HC, Liu ZP. Gene cloning and characterization of a cold-adapted beta-glucosidase belonging to glycosyl hydrolase family 1 from a psychrotolerant bacterium Micrococcus antarcticus. Enzyme Microb Technol 2011;49: 94–99. 10.1016/j.enzmictec.2011.03.001 PubMed DOI

Anderson I, Abt B, Lykidis A, Klenk HP, Kyrpides N, Ivanova N. Genomics of aerobic Cellulose utilization systems in Actinobacteria. PLOS One 2012;7: e39331 10.1371/journal.pone.0039331 PubMed DOI PMC

Enkhbaatar B, Temuujin U, Lim JH, Chi WJ, Chang YK, Hong SK. Identification and characterization of a Xyloglucan-Specific Family 74 Glycosyl Hydrolase from Streptomyces coelicolor A3(2). Appl Environ Microbiol. 2012;78: 607–611. 10.1128/AEM.06482-11 PubMed DOI PMC

Zhang F, Hu SN, Chen JJ, Lin LB, Wei YL, Tang SK, et al. Purification and partial characterisation of a thermostable xylanase from salt-tolerant Thermobifida halotolerans YIM 90462(T). Process Biochem. 2012;47: 225–228. 10.1016/j.procbio.2011.10.032 DOI

Větrovský T, Steffen KT, Baldrian P. Potential of cometabolic transformation of polysaccharides and lignin in lignocellulose by soil Actinobacteria. PLoS One. 2014;9: e89108 10.1371/journal.pone.0089108 PubMed DOI PMC

Jolles P, Muzzarelli RAA. Preface In: Jolles P, Muzzarelli RAA, editors. Chitin and Chitinases. Basel: Birkhäuser Verlag; 1999.

Bartnicki-Garcia S. Cell wall chemistry, morphogenesis, and taxonomy of fungi. Annu Rev Microbiology. 1968;22: 87–108. 10.1146/annurev.mi.22.100168.000511 PubMed DOI

Jha S, Modi HA, Jha CK. Characterization of extracellular chitinase produced from Streptomyces rubiginosus isolated from rhizosphere of Gossypium sp. Cogent Food & Agriculture 2016;2: 1198225 10.1080/23311932.2016.1198225 DOI

Kawase T, Saito A, Sato T, Kanai R, Fujii T, Nikaidou N., et al. Distribution and phylogenetic analysis of family 19 Chitinases in Actinobacteria. Appl Environ Microbiol. 2004;70: 1135–1144. 10.1128/AEM.70.2.1135-1144.2004 PubMed DOI PMC

Brabcová V, Nováková M, Davidová A, Baldrian P. Dead fungal mycelium in forest soil represents a decomposition hotspot and a habitat for a specific microbial community. New Phytol. 2016;201: 1369–1381. 10.1111/nph.13849 PubMed DOI

López-Mondéjar R, Brabcová V, Štursová M, Davidová A, Jansa J, Cajthaml T, Baldrian P. Decomposer food web in a deciduous forest shows high share of generalist microorganisms and importance of microbial biomass recycling. ISME J. 2018;12: 1768–1778. 10.1038/s41396-018-0084-2 PubMed DOI PMC

Brabcová V, Štursová M, Baldrian P. Nutrient content affects the turnover of fungal biomass in forest topsoil and the composition of associated microbial communities. Soil Biol Biochem. 2018;118: 187–198. 10.1016/j.soilbio.2017.12.012 DOI

Traving SJ, Thygesen UH, Riemann L Stedmon CA. A model of extracellular enzymes in free-living microbes: which strategy pays off? Appl Environ Microbiol. 2015;81: 7385–7393. 10.1128/AEM.02070-15 PubMed DOI PMC

Burns RG. How do microbial extracellular enzymes locate and degrade natural and synthetic polymers in soil In: Xu J, Huang PM, editors. Molecular environmental soil science at the interfaces in the Earth’s critical zone., Berlin, Heidelberg: Springer–Verlag; 2010. pp 294–297.

Burns RG. Enzyme activity in soil: Location and a possible role in microbial ecology. Soil Biol Biochem. 1982;14: 423–427. 10.1016/0038-0717(82)90099-2 DOI

Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, et al. Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biol Biochem. 2013;58: 216–234. 10.1016/j.soilbio.2012.11.009 DOI

Reintjes G, Arnosti C, Fuchs BM, Amman R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 2017;11: 1640–1650. 10.1038/ismej.2017.26 PubMed DOI PMC

Fernández-González AJ, Martínez-Hidalgo P, Cobo-Díaz JF, Villadas PJ, Martínez-Molina E, Toro N, et al. The rhizosphere microbiome of burned holm-oak: potential role of the genus Arthrobacter in the recovery of burned soils. Sci Rep 7 2017; 6008 10.1038/s41598-017-06112-3 PubMed DOI PMC

Cobo-Díaz JF, Fernández-González AJ, Villadas PJ, Robles AB, Toro N, Fernández-López M. Metagenomic assessment of the potential microbial nitrogen pathways in the rhizosphere of a Mediterranean forest after a wildfire. Microb Ecol. 2015;69: 895–904. 10.1007/s00248-015-0586-7 PubMed DOI

Cobo-Díaz JF, Fernández-González AJ, Villadas PJ, Toro N, Tringe SG, Fernández-López M. Taxonomic and functional diversity of Quercus pyrenaica rhizospheric microbiome in Mediterranean mountains. Forests. 2017;8: 390 10.3390/f8100390 DOI

Lasa AV, Fernández-González AJ, Villadas PJ, Toro N, Fernández-López M. Metabarcoding reveals that rhizospheric microbiota of Quercus pyrenaica is composed by a relatively small number of bacterial taxa highly abundant. Sci Rep. 2019;1695 10.1038/s41598-018-38123-z PubMed DOI PMC

Eberspächer J, Lingens F. The genus Phenylobacterium. In: Prokaryotes. 2006;5: 250–256.

Mühling M, Woolven-Allen J, Murrel JC, Joint I. Improved group-specific PCR primers for denaturing gradient gel electrophoresis analysis of the genetic diversity of complex microbial communities. ISME J. 2008;2: 379–392. 10.1038/ismej.2007.97 PubMed DOI

Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991;173: 687–703. 10.1128/jb.173.2.697-703.1991 PubMed DOI PMC

Rivas R, García-Fraile P, Mateos PF, Martínez-Molina E, Velázquez E. Characterization of xylanolytic bacteria present in the bract phyllosphere of the date palm Phoenix dactylifera. Lett Appl Microbiol. 2007;44: 181–187. 10.1111/j.1472-765X.2006.02050.x PubMed DOI

Paik J, Low NH, Ingledew WM. Malt Extract: Relationship of Chemical Composition to Fermentability. J Am Soc Brew Chem. 1991;49: 8–13. 10.1094/ASBCJ-49-0008 DOI

Evans DE, Redd K, Haraysmow SE, Elvig N, Metz N, Koutoulis A. The Influence of Malt Quality on Malt Brewing and Barley Quality on Barley Brewing with Ondea Pro, Compared by Small-Scale Analysis. J Am Soc Brew Chem. 2014;72: 192–207. 10.1094/ASBCJ-2014-0630-01 DOI

Houfani AA, Větrovský T, Baldrian P, Benallaoua S. Efficient screening of potential cellulases and hemicellulases produced by Bosea sp. FBZP-16 using the combination of enzyme assays and genome analysis. World J Microbiol Biotechnol. 2017;33: 29 10.1007/s11274-016-2198-x PubMed DOI

Baldrian P, Voříšková J, Dobiášová P, Merhautová V, Lisá L, Valášková V. Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant Soil. 2011;338: 111–125. 10.1007/s11104-010-0324-3 DOI

Mašinová T, Yurkov A, Baldrian P. Forest soil yeasts: potential and the utilization of carbon sources. Fungal Ecol. 2018;34: 10–19. 10.1016/j.funeco.2018.03.005 DOI

Baldrian P. Microbial enzyme-catalized processes in soils and their analysis. Plant Soil Environ. 2009; 55: 370–378. 10.17221/134/2009-PSE DOI

R Core Team (2017) R: A Language and Environment for Statistical Computing R Foundation for Statistical Computing, Vienna, Austria.

Eichlerová I, Homolka L, Žifčáková L, Lisá L, Dobiášová P, Baldrian P. Enzymatic systems involved in the decomposition reflects the ecology and taxonomy of saprotrophic fungi. Fungal Ecol. 2015;13: 10–22. 10.1016/j.funeco.2014.08.002 DOI

van den Brink J, de Vries RP. Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol. 2011;91:.1477–1492. 10.1007/s00253-011-3473-2 PubMed DOI PMC

van der Wal A, Geydan TD, Kuyper WD, de Boer W. A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiol Rev. 2013;37: 477–494. 10.1111/1574-6976.12001 PubMed DOI

Mulet M, Lalucat J, García-Valdés E. DNA sequence-based analysis of the Pseudomonas species. Environ Microbiol 2010;12: 1513–1530. 10.1111/j.1462-2920.2010.02181.x PubMed DOI

Allison SD. Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecol Lett. 2005;8: 626–635. 10.1111/j.1461-0248.2005.00756.x DOI

Robledo M, Jiménez-Zurdo JI, Velázquez E, Trujillo ME, Zurdo-Piñeiro JL, Ramírez-Bahena MH, et al. Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. PNAS. 2008;105: 7064–7069. 10.1073/pnas.0802547105 PubMed DOI PMC

López-Mondéjar R, Zühlke D, Větrovský T, Becher D, Riedel K, Baldrian P. Decoding the complete arsenal for cellulose and hemicellulose deconstruction in the highly efficient cellulose decomposer Paenibacillus O199. Biotechnol Biofuels. 2016;9: 104 10.1186/s13068-016-0518-x PubMed DOI PMC

Valášková V, Baldrian P. Estimation of bound and free fractions of lignocellulose-degrading enzymes of wood-rotting fungi Pleurotus ostreatus, Trametes versicolor and Piptoporus betulinus. Res Microbiol. 2006;157: 119–124. 10.1016/j.resmic.2005.06.004 PubMed DOI

Suen G, Weimer PJ, Stevenson DM, Aylward FO, Boyum J, Deneke J, et al. The complete genome sequence of Fibrobacter succinogenes S85 reveals a cellulolytic and metabolic specialist. PLos One. 2011;6: e18814 10.1371/journal.pone.0018814 PubMed DOI PMC

Vodovnik M, Duncan SH, Reid MD, Cantla L, Turner K, Parkhill J, et al. Expression of cellulosome components and type IV pili within the extracellular proteome of Ruminococcus flavefaciens 007. PLos One. 2013;8: e65333 10.1371/journal.pone.0065333 PubMed DOI PMC

Hallmann AQ, Kloeppler JW, Benhamou N. Bacterial endophytes in cotton: mechanisms of entering the plant. Can J Microbiol. 1997;43: 577–582. 10.1139/m97-081 DOI

Shu Z, Lin H, Shi S, Mu X, Huang J. Cell-bound lipases from Burkholderia sp. ZYB002: gene sequence analysis, expression, enzymatic characterization and 3D structural model. BMC Biotechnol. 2016;16, 38 10.1186/s12896-016-0269-6 PubMed DOI PMC

Reilly TJ, Chance DL, Calcutt MJ, Tanner JJ, Felts RL, Waller SC, et al. Characterization of a unique class C acid phosphatase from Clostridium perfringens. Appl Environ Microbiol. 2009;75: 3745–3754. 10.1128/AEM.01599-08 PubMed DOI PMC

Vrba J, Nedoma J, Šimek K, Seda J. Microbial decomposition of polymeric organic matter related to plankton development in a reservoir: activity of α-, β-glucosidase, and β-N-acetylglucosaminidase and uptake of N-acetylglucosamine. Arch Hydrobiol. 1992;126: 193–211.

Keith SD, Arnosti C. Extracellular enzyme activity in a river-bay-shelf transect: variations in polysaccharide hydrolysis rates with substrate and size class. Aquat Microb Ecol. 2001;24: 243–253. 10.3354/ame024243 DOI

Berlemont R, Martiny AC. Phylogenetic distribution of potential cellulases in bacteria. Appl Environ Microbiol. 2013;79: 1545–1554. 10.1128/AEM.03305-12 PubMed DOI PMC

Goldfarb KC, Karaoz U, Hanson CA, Santee CA, Bradford MA, Treseder KK, et al. Differential growth responses of soil bacterial taxa to carbon substrates of varying chemical recalcitrance. Front Microbiol. 2011;2: 94 10.3389/fmicb.2011.00094 PubMed DOI PMC

Ulrich A, Klimke G, Wirth S. Diversity and activity of cellulose-decomposing bacteria, isolated from a sandy and a loamy soil after long-term manure application. Microb Ecol. 2008;55: 512–522. 10.1007/s00248-007-9296-0 PubMed DOI

Sigurbjörnsdóttir MA, Vilhelmsson O. Selective isolation of potentially phosphate-mobilizing, biosurfactant-producing and biodegradative bacteria associated with a sub-Arctic, terricolous lichen, Peltigera membranacea. FEMS Microbiol Ecol. 2016;92: fiw90 10.1093/femsec/fiw090 PubMed DOI

Carrim AJI, Barbosa EC, Vieira JDG. Enzymatic activity of endophytic bacterial isolates of Jacaranda decurrens Cham. (Carobinha-do-campo). Braz Arch Biol Technol. 2006;49: 353–359. 10.1590/S1516-89132006000400001 DOI

Naveed M, Mitter B, Yousaf S, Pastar M, Afzal M, Sessitsch A. The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils. 2014;50: 249–262. 10.1007/s00374-013-0854-y DOI

Castro RA, Quecine MC, Lacava PT, Batista BD, Luvizotto DM, Marcon J et al. Isolation and enzyme bioprospection of endophytic bacteria associated with plants of Brazilian mangrove ecosystem. SpringerPlus. 2014;3: 382 10.1186/2193-1801-3-382 PubMed DOI PMC

Bergkemper F, Kublik S, Lang F, Krüger J, Vestergaard G, Schloter M, et al. Novel oligonucleotide primers reveal a high diversity of microbes which drive phosphorous turnover in soil. J Microbiol Methods. 2016;125: 91–97.doi: 10.1016/j.mimet.2016.04.011 10.1016/j.mimet.2016.04.011 PubMed DOI

Huang Z, Bao YY, Yuan TT, Wang GX, He LY, Sheng XF (2015) Arthrobacter nanjingensis sp. nov., a mineral-weathering bacterium isolated from forest soil. Int J Syst Evol Microbiol. 2015;65: 365–369. 10.1099/ijs.0.069492-0 PubMed DOI

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