Terracidiphilus gabretensis gen. nov., sp. nov., an Abundant and Active Forest Soil Acidobacterium Important in Organic Matter Transformation

. 2016 Jan 15 ; 82 (2) : 560-9. [epub] 20151106

Jazyk angličtina Země Spojené státy americké Médium electronic-print

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26546425

Understanding the activity of bacteria in coniferous forests is highly important, due to the role of these environments as a global carbon sink. In a study of the microbial biodiversity of montane coniferous forest soil in the Bohemian Forest National Park (Czech Republic), we succeeded in isolating bacterial strain S55(T), which belongs to one of the most abundant operational taxonomic units (OTUs) in active bacterial populations, according to the analysis of RNA-derived 16S rRNA amplicons. The 16S rRNA gene sequence analysis showed that the species most closely related to strain S55(T) include Bryocella elongata SN10(T) (95.4% identity), Acidicapsa ligni WH120(T) (95.2% identity), and Telmatobacter bradus TPB6017(T) (95.0% identity), revealing that strain S55(T) should be classified within the phylum Acidobacteria, subdivision 1. Strain S55(T) is a rod-like bacterium that grows at acidic pH (3 to 6). Its phylogenetic, genotypic, phenotypic, and chemotaxonomic characteristics indicate that strain S55(T) corresponds to a new genus within the phylum Acidobacteria; thus, we propose the name Terracidiphilus gabretensis gen. nov., sp. nov. (strain S55(T) = NBRC 111238(T) = CECT 8791(T)). This strain produces extracellular enzymes implicated in the degradation of plant-derived biopolymers. Moreover, analysis of the genome sequence of strain S55(T) also reveals the presence of enzymatic machinery required for organic matter decomposition. Soil metatranscriptomic analyses found 132 genes from strain S55(T) being expressed in the forest soil, especially during winter. Our results suggest an important contribution of T. gabretensis S55(T) in the carbon cycle in the Picea abies coniferous forest.

Zobrazit více v PubMed

Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS. 2002. Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577. doi:10.1128/MMBR.66.3.506-577.2002. PubMed DOI PMC

Burns RG. 1978. Soil enzymes. Academic Press, London, United Kingdom.

Baldrian P. 2006. Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30:215–242. doi:10.1111/j.1574-4976.2005.00010.x. PubMed DOI

Osono T. 2007. Ecology of ligninolytic fungi associated with leaf litter decomposition. Ecol Res 22:955–974. doi:10.1007/s11284-007-0390-z. DOI

Wilson DB. 2008. Three microbial strategies for plant cell wall degradation, p 289–297. In Wiegel J, Maier RJ, Adams MWW (ed), Incredible anaerobes: from physiology to genomics to fuels. Blackwell, Oxford, United Kingdom. PubMed

Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A. 2013. Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234. doi:10.1016/j.soilbio.2012.11.009. DOI

Janssen PH. 2006. Identifying the dominant soil bacterial taxa in libraries of 16S rRNA and 16S rRNA genes. Appl Environ Microbiol 72:1719–1728. doi:10.1128/AEM.72.3.1719-1728.2006. PubMed DOI PMC

Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N. 2009. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453. doi:10.1038/ismej.2008.127. PubMed DOI PMC

Männistö MK, Tiirola M, Häggblom MM. 2007. Bacterial communities in Arctic fields of Finnish Lapland are stable but highly pH-dependent. FEMS Microbiol Ecol 59:452–465. doi:10.1111/j.1574-6941.2006.00232.x. PubMed DOI

Kuske CR, Barns SM, Busch JD. 1997. Diverse uncultivated bacterial groups from soils of the arid southwestern United States that are present in many geographic regions. Appl Environ Microbiol 63:3614–3621. PubMed PMC

Barns SM, Takala SL, Kuske CR. 1999. Wide distribution and diversity of members of the bacterial kingdom Acidobacterium in the environment. Appl Environ Microbiol 65:1731–1737. PubMed PMC

Dunbar J, Takala S, Barns SM, Davis JA, Kuske CR. 1999. Levels of bacterial community diversity in four arid soils compared by cultivation and 16S rRNA gene cloning. Appl Environ Microbiol 65:1662–1669. PubMed PMC

Dunbar J, Barns SM, Ticknor LO, Kuske CR. 2002. Empirical and theoretical bacterial diversity in four Arizona soils. Appl Environ Microbiol 68:3035–3045. doi:10.1128/AEM.68.6.3035-3045.2002. PubMed DOI PMC

Okamura K, Kawai A, Yamada T, Hiraishi A. 2011. Acidipila rosea gen. nov., sp. nov., an acidophilic chemoorganotrophic bacterium belonging to the phylum Acidobacteria. FEMS Ecol Lett 317:138–142. PubMed

Koch IH, Gich F, Dunfield PF, Overmann J. 2008. Edaphobacter modestus gen. nov., sp. nov., and Edaphobacter aggregans sp. nov., acidobacteria isolated from alpine and forests soils. Int J Syst Evol Microbiol 58:1114–1122. PubMed

Pankratov TA, Dedysh SV. 2010. Granulicella paludicola gen. nov., sp. nov., Granulicella pectinivorans sp. nov., Granulicella aggregans sp. nov., and Granulicella rosea sp. nov., acidophilic, polymer-degrading acidobacteria from Sphagnum peat bogs. Int J Syst Evol Microbiol 60:2951–2959. PubMed

Dedysh SN, Kulichevskaya IS, Serkebaeva YM, Mityaeva MA, Sorokin VV, Suzina NE, Rijpstra WIC, Sinninghe Damsté JS. 2008. 2011. Bryocella elongata gen. nov., sp. nov., a member of subdivision 1 of the Acidobacteria isolated from a methanotrophic enrichment culture, and emended description of Edaphobacter aggregans Koch et al. Int J Syst Evol Microbiol 62:654–664. doi:10.1099/ijs.0.031898-0. PubMed DOI

Männistö MK, Rawat S, Starovoytov V, Häggblom MM. 2012. Granulicella arctica sp. nov., Granulicella mallensis sp. nov., Granulicella tundricola sp. nov., and Granulicella sapmiensis sp. nov., novel acidobacteria from tundra soil. Int J Syst Evol Microbiol 62:2097–2106. doi:10.1099/ijs.0.031864-0. PubMed DOI

Pankratov TA, Kirsanova LA, Kaparullina EN, Kevbrin VV, Dedysh SN. 2012. Telmatobacter bradus gen. nov., sp. nov., a cellulolytic facultative anaerobe from subdivision 1 of the Acidobacteria, and emended description of Acidobacterium capsulatum Kishimoto et al. 1991. Int J Syst Evol Microbiol 62:430–437. doi:10.1099/ijs.0.029629-0. PubMed DOI

Kulichevskaya IS, Kostina LA, Valášková V, Rijpstra WIC, Sinninghe Damsté JS, de Boer W, Dedysh SN. 2012. Acidicapsa borealis gen. nov., sp. nov. and Acidicapsa ligni sp. nov., subdivision 1 Acidobacteria from Sphagnum peat and decaying wood. Int J Syst Evol Microbiol 62:1512–1520. doi:10.1099/ijs.0.034819-0. PubMed DOI

Ludwig W, Bauer SH, Bauer M, Held I, Kirchhof G, Schulze R, Huber I, Spring S, Hartmann A, Schleifer KH. 1997. Detection and in situ identification of representatives of a widely distributed new bacterial phylum. FEMS Microbiol Lett 153:181–190. doi:10.1111/j.1574-6968.1997.tb10480.x. PubMed DOI

Fierer N, Morse JL, Berthrong ST, Bernhardt ES, Jackson RB. 2007. Environmental controls on the landscape-scale biogeography of stream bacterial communities. Ecology 88:2162–2173. doi:10.1890/06-1746.1. PubMed DOI

Foesel BU, Nägele V, Naether A, Wüst PK, Weiner J, Bonkowski M, Lohaus G, Polle A, Alt F, Oelmann Y, Fischer M, Friedrich MW, Overmann J. 2014. Determinants of Acidobacteria activity inferred from the relative abundances of 16S rRNA transcripts in German grasslands and forest soils. Environ Microbiol 16:658–675. doi:10.1111/1462-2920.12162. PubMed DOI

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

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

Rawat SR, Männistö MK, Bromberg Y, Häggblom MM. 2012. Comparative genomic and physiological analysis provide insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils. FEMS Microbiol Ecol 82:341–355. doi:10.1111/j.1574-6941.2012.01381.x. PubMed DOI

Žifčáková L, Větrovský T, Howe A, Baldrian P. Microbial activity in forest soil reflects the changes in ecosystem properties between summer and winter. Environ Microbiol, in press. doi:10.1111/1462-2920.13026. 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, in press. doi:10.1007/s00374-015-1072-6. DOI

Baldrian P, Kolařík M, Štursová M, Kopecký J, Valášková V, Větrovský T, Žifčáková L, Šnajdr J, Rídl J, Vlček C, Voříšková J. 2012. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME J 6:248–258. doi:10.1038/ismej.2011.95. PubMed DOI PMC

Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA. 2008. The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386. doi:10.1186/1471-2105-9-386. PubMed DOI PMC

Větrovský T, Baldrian P. 2013. Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol Fertil Soils 49:1027–1037.

Větrovský T, Baldrian P. 2013. The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS One 8:e57923. doi:10.1371/journal.pone.0057923. PubMed DOI PMC

Sait M, Hugenholtz P, Janssen PH. 2002. Cultivation of globally distributed soil bacteria from phylogenetic lineages previously only detected in cultivation-independent surveys. Environ Microbiol 4:654–666. doi:10.1046/j.1462-2920.2002.00352.x. PubMed DOI

George IF, Hartmann M, Liles MR, Agathos SN. 2011. Recovery of as-yet-uncultured soil Acidobacteria on dilute soil media. Appl Environ Microbiol 77:8184–8188. doi:10.1128/AEM.05956-11. PubMed DOI PMC

García-Fraile P, Chudíčková M, Benada O, Pikula J, Kolařík M. 2015. Serratia myotis sp. nov. and Serratia vespertilionis sp. nov., isolated from bats hibernating in caves in the Czech Republic. Int J Syst Evol Microbiol 65:90–94. doi:10.1099/ijs.0.066407-0. PubMed DOI

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

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2. PubMed DOI

Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J. 2012. Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721. doi:10.1099/ijs.0.038075-0. PubMed DOI

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121. PubMed DOI PMC

Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. doi:10.1093/nar/22.22.4673. PubMed DOI PMC

Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404. PubMed DOI

Kimura M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. doi:10.1007/BF01731581. PubMed DOI

Rogers JS, Swofford DL. 1998. A fast method for approximating maximum likelihoods of phylogenetic trees from nucleotide sequences. Syst Biol 47:77–89. doi:10.1080/106351598261049. PubMed DOI

Saitou N, Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetics trees. Mol Biol Evol 4:406–425. PubMed

Šnajdr J, Valášková V, Merhautová V, Herinková J, Cajthaml T, Baldrian P. 2008. Spatial variability of enzyme activities and microbial biomass in the upper layers of Quercus petraea forest soil. Soil Biol Biochem 40:2068–2075. doi:10.1016/j.soilbio.2008.01.015. DOI

Doetsch RN. 1981. Determinative methods of light microscopy, p 21–33. In Gerdhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, Krieg NR, Phillips GB (ed), Manual of methods for general bacteriology. American Society for Microbiology, Washington, DC.

Fassel TA, Schaller MJ, Remsen CC. 1992. Comparison of alcian blue and ruthenium red effects on preservation of outer envelope ultrastructure in methanotrophic bacteria. Microsc Res Tech 20:87–94. doi:10.1002/jemt.1070200109. PubMed DOI

Kellenberger E, Sechaud J, Ryter A. 1959. Electron microscopical studies of phage multiplication. IV. The establishment of the DNA pool of vegetative phage and the maturation of phage particles. Virology 8:478–498. PubMed

Reynolds ES. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212. doi:10.1083/jcb.17.1.208. PubMed DOI PMC

Kovács N. 1956. Eine vereinfachte Methode zum Nachweis der indolbildung durch Bakterien. Z Immunitätsforschung 55:311–315.

Nagpure A, Gupta RK. 2013. Purification and characterization of an extracellular chitinase from antagonistic Streptomyces violaceusniger. J Basic Microbiol 53:429–439. doi:10.1002/jobm.201100648. PubMed DOI

Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829. doi:10.1101/gr.074492.107. PubMed DOI PMC

Darling AE, Jospin G, Lowe E, Matsen FA IV, Bik HM, Eisen JA. 2014. PhyloSift: phylogenetic analysis of genomes and metagenomes. PeerJ 2:e243. doi:10.7717/peerj.243. PubMed DOI PMC

Yin YB, Mao XZ, Yang JC, Chen X, Mao FL, Xu Y. 2012. dbCAN: a Web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40:W445–W451. doi:10.1093/nar/gks479. PubMed DOI PMC

Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu C, Zafar N, Zhou, Kuske CR. 2009. Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056. doi:10.1128/AEM.02294-08. PubMed DOI PMC

Challacombe JF, Eichorst SA, Hauser L, Land M, Xie G, Kuske CR. 2011. Biological consequences of ancient gene acquisition and duplication in the large genome of “Candidatus Solibacter usitatus” Ellin6076. PLoS One 6:e24882. doi:10.1371/journal.pone.0024882. PubMed DOI PMC

Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S. 2012. Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762. doi:10.1007/s00374-012-0723-0. DOI

Wang M, Liu K, Dai L, Zhang J, Fang X. 2013. The structural and biochemical basis for cellulose biodegradation. J Chem Technol Biotechnol 88:491–500. doi:10.1002/jctb.3987. DOI

Pankratov TA, Ivanova AO, Dedysh SN, Llesack W. 2011. Bacterial populations and environmental factors controlling cellulose degradation in an acidic Sphagnum peat. Environ Microbiol 13:1800–1814. doi:10.1111/j.1462-2920.2011.02491.x. PubMed DOI

van den Brink J, de Vries RP. 2011. Fungal enzyme sets for plant polysaccharide degradation. Appl Microbiol Biotechnol 91:1477–1149. doi:10.1007/s00253-011-3473-2. PubMed DOI PMC

Fontaine S, Mariotti A, Abbadie L. 2003. The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843. doi:10.1016/S0038-0717(03)00123-8. DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...