Deadwood-Inhabiting Bacteria Show Adaptations to Changing Carbon and Nitrogen Availability During Decomposition

. 2021 ; 12 () : 685303. [epub] 20210617

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34220772

Deadwood decomposition is responsible for a significant amount of carbon (C) turnover in natural forests. While fresh deadwood contains mainly plant compounds and is extremely low in nitrogen (N), fungal biomass and N content increase during decomposition. Here, we examined 18 genome-sequenced bacterial strains representing the dominant deadwood taxa to assess their adaptations to C and N utilization in deadwood. Diverse gene sets for the efficient decomposition of plant and fungal cell wall biopolymers were found in Acidobacteria, Bacteroidetes, and Actinobacteria. In contrast to these groups, Alphaproteobacteria and Gammaproteobacteria contained fewer carbohydrate-active enzymes and depended either on low-molecular-mass C sources or on mycophagy. This group, however, showed rich gene complements for N2 fixation and nitrate/nitrite reduction-key assimilatory and dissimilatory steps in the deadwood N cycle. We show that N2 fixers can obtain C independently from either plant biopolymers or fungal biomass. The succession of bacteria on decomposing deadwood reflects their ability to cope with the changing quality of C-containing compounds and increasing N content.

Zobrazit více v PubMed

Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., et al. . (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402. 10.1093/nar/25.17.3389 PubMed DOI PMC

Anderson-Teixeira K. J., Davies S. J., Bennett A. C., Muller-landau H. C., Wright S. J. (2015). CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change. Glob. Change Biol. 21, 528–549. 10.1111/gcb.12712 PubMed DOI

Baldrian P., Zrustová P., Tláskal V., Davidová A., Merhautová V., Vrška T. (2016). Fungi associated with decomposing deadwood in a natural beech-dominated forest. Fungal Ecol. 23, 109–122. 10.1016/j.funeco.2016.07.001 DOI

Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Alexander S., Kulikov A. S., et al. . (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477. 10.1089/cmb.2012.0021 PubMed DOI PMC

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

Berlemont R., Martiny A. C. (2015). Genomic potential for polysaccharide deconstruction in Bacteria. Appl. Environ. Microbiol. 81, 1513–1519. 10.1128/AEM.03718-14 PubMed DOI PMC

Bowers R. M., Kyrpides N. C., Stepanauskas R., Harmon-Smith M., Doud D., Reddy T. B. K., et al. . (2017). Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat. Biotechnol. 35, 725–731. 10.1038/nbt.3893 PubMed DOI PMC

Brabcová V., Nováková M., Davidová A., Baldrian P. (2016). Dead fungal mycelium in forest soil represents a decomposition hotspot and a habitat for a specific microbial community. New Phytol. 210, 1369–1381. 10.1111/nph.13849 PubMed DOI

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

Brunner A., Kimmins J. P. (2003). Nitrogen fixation in coarse woody debris of Thuja plicata and Tsuga heterophylla forests on northern Vancouver Island. Can. J. For. Res. 33, 1670–1682. 10.1139/x03-085 DOI

Capella-Gutiérrez S., Silla-Martínez J. M., Gabaldón T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973. 10.1093/bioinformatics/btp348 PubMed DOI PMC

Christofides S. R., Hiscox J., Savoury M., Boddy L., Weightman A. J. (2019). Fungal control of early-stage bacterial community development in decomposing wood. Fungal Ecol. 42:100868. 10.1016/j.funeco.2019.100868 DOI

de Mendiburu F. (2017). Agricolae: Statistical Procedures for Agricultural Research. R package version 1.2–4.

Eddy S. R. (2011). Accelerated profile HMM searches. PLoS Comput. Biol. 7:e1002195. 10.1371/journal.pcbi.1002195 PubMed DOI PMC

Edgar R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797. 10.1093/nar/gkh340 PubMed DOI PMC

Filley T. R., Cody G. D., Goodell B., Jellison J., Noser C., Ostrofsky A. (2002). Lignin demethylation and polysaccharide decomposition in spruce sapwood degraded by brown rot fungi. Org. Geochem. 33, 111–124. 10.1016/S0146-6380(01)00144-9 DOI

Folman L. B., Gunnewiek P. J. A. K., Boddy L., de Boer W. (2008). Impact of white-rot fungi on numbers and community composition of bacteria colonizing beech wood from forest soil. FEMS Microbiol. Ecol. 63, 181–191. 10.1111/j.1574-6941.2007.00425.x PubMed DOI

Gallardo C. A., Baldrian P., López-mondéjar R. (2021). Litter-inhabiting fungi show high level of specialization towards biopolymers composing plant and fungal biomass. Biol. Fertil. Soils 57, 77–88. 10.1007/s00374-020-01507-3 DOI

Hervé V., Ketter E., Pierrat J.-C., Gelhaye E., Frey-Klett P. (2016). Impact of Phanerochaete chrysosporium on the functional diversity of bacterial communities associated with decaying wood. PLoS ONE 11:e0147100. 10.1371/journal.pone.0147100 PubMed DOI PMC

Hervé V., Le Roux X., Uroz S., Gelhaye E., Frey-Klett P. (2013). Diversity and structure of bacterial communities associated with Phanerochaete chrysosporium during wood decay. Environ. Microbiol. 16, 2238–2252. 10.1111/1462-2920.12347 PubMed DOI

Hoppe B., Krüger D., Kahl T., Arnstadt T., Buscot F., Bauhus J., et al. . (2015). A pyrosequencing insight into sprawling bacterial diversity and community dynamics in decaying deadwood logs of Fagus sylvatica and Picea abies. Sci. Rep. 5:9456. 10.1038/srep09456 PubMed DOI PMC

Hyatt D., Chen G. L., LoCascio P. F., Land M. L., Larimer F. W., Hauser L. J. (2010). Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11:119. 10.1186/1471-2105-11-119 PubMed DOI PMC

Johnston S. R., Boddy L., Weightman A. J. (2016). Bacteria in decomposing wood and their interactions with wood-decay fungi. FEMS Microbiol. Ecol. 92:fiw179. 10.1093/femsec/fiw179 PubMed DOI

Johnston S. R., Hiscox J., Savoury M., Boddy L., Weightman A. J. (2019). Highly competitive fungi manipulate bacterial communities in decomposing beech wood (Fagus sylvatica). FEMS Microbiol. Ecol. 95:fiy225. 10.1093/femsec/fiy225 PubMed DOI PMC

Katoh K., Rozewicki J., Yamada K. D. (2018). MAFFT online service: multiple sequence alignment, interactive sequence choice, and visualization. Brief. Bioinform. 20, 1160–1166. 10.1093/bib/bbx108 PubMed DOI PMC

Král K., Janík D., Vrška T., Adam D., Hort L., Unar P., et al. . (2010). Local variability of stand structural features in beech dominated natural forests of Central Europe: Implications for sampling. For. Ecol. Manage. 260, 2196–2203. 10.1016/j.foreco.2010.09.020 DOI

Lagesen K., Hallin P., Rødland E. A., Stærfeldt H. H., Rognes T., Ussery D. W. (2007). RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 35, 3100–3108. 10.1093/nar/gkm160 PubMed DOI PMC

Lane D. J. (1991). “16S/23S rRNA sequencing,” in Nucleic Acid Techniques in Bacterial Systematics, eds Stackebrandt E., Goodfellow M. (New York, NY: Wiley; ), 115–175.

Langmead B., Salzberg S. L. (2013). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359. 10.1038/nmeth.1923 PubMed DOI PMC

Langmead B., Trapnell C., Pop M., Salzberg S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. 10.1186/gb-2009-10-3-r25 PubMed DOI PMC

Lasa A. V., Mašínová T., Baldrian P., Fernández-López M. (2019). Bacteria from the endosphere and rhizosphere of Quercus spp. use mainly cell wall-associated enzymes to decompose organic matter. PLoS ONE 14:e0214422. 10.1371/journal.pone.0214422 PubMed DOI PMC

Leahy J. G., Batchelor P. J., Morcomb S. M. (2003). Evolution of the soluble diiron monooxygenases. FEMS Microbiol. Rev. 27, 449–479. 10.1016/S0168-6445(03)00023-8 PubMed DOI

Lee M. D. (2019). GToTree: a user-friendly workflow for phylogenomics. Bioinformatics 35, 4162–4164. 10.1093/bioinformatics/btz188 PubMed DOI PMC

Lenhart K., Bunge M., Ratering S., Neu T. R., Schüttmann I., Greule M., et al. . (2012). Evidence for methane production by saprotrophic fungi. Nat. Commun. 3:1046. 10.1038/ncomms2049 PubMed DOI

Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., et al. . (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079. 10.1093/bioinformatics/btp352 PubMed DOI PMC

Lladó S. F., Větrovský T., Baldrian P. (2019). Tracking of the activity of individual bacteria in temperate forest soils shows guild-specific responses to seasonality. Soil Biol. Biochem. 135, 275–282. 10.1016/j.soilbio.2019.05.010 DOI

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

Lombard V., Golaconda Ramulu H., Drula E., Coutinho P. M., Henrissat B. (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490–D495. 10.1093/nar/gkt1178 PubMed DOI PMC

López-Mondéjar R., Algora C., Baldrian P. (2019). Lignocellulolytic systems of soil bacteria: a vast and diverse toolbox for biotechnological conversion processes. Biotechnol. Adv. 37, 399–404. 10.1016/j.biotechadv.2019.03.013 PubMed DOI

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

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

Madin J. S., Nielsen D. A., Brbic M., Corkrey R., Danko D., Edwards K., et al. . (2020). A synthesis of bacterial and archaeal phenotypic trait data. Sci. Data 7:170. 10.1038/s41597-020-0497-4 PubMed DOI PMC

Martin A. R., Domke G. M., Doraisami M., Thomas S. C. (2021). Carbon fractions in the world's dead wood. Nat. Commun. 12:889. 10.1038/s41467-021-21149-9 PubMed DOI PMC

Mieszkin S., Richet P., Bach C., Lambrot C., Augusto L., Buée M., et al. . (2021). Oak decaying wood harbors taxonomically and functionally different bacterial communities in sapwood and heartwood. Soil Biol. Biochem. 155:108160. 10.1016/j.soilbio.2021.108160 DOI

Moll J., Kellner H., Leonhardt S., Stengel E., Dahl A., Buscot F., et al. . (2018). Bacteria inhabiting deadwood of 13 tree species reveal great heterogeneous distribution between sapwood and heartwood. Environ. Microbiol. 20, 3744–3756. 10.1111/1462-2920.14376 PubMed DOI

Nayfach S., Roux S., Seshadri R., Udwary D., Varghese N., Schulz F., et al. . (2020). A genomic catalog of Earth's microbiomes. Nat. Biotechnol. 39:520. 10.1038/s41587-020-00769-4 PubMed DOI PMC

Nelson M. B., Martiny A. C., Martiny J. B. H. (2016). Global biogeography of microbial nitrogen-cycling traits in soil. Proc. Natl. Acad. Sci. U.S.A. 113, 8033–8040. 10.1073/pnas.1601070113 PubMed DOI PMC

Odriozola I., Abrego N., Tláskal V., Zrustová P., Morais D., Větrovský T., et al. . (2021). Fungal communities are important determinants of bacterial community composition in deadwood. mSystems 6, e01017–e01020. 10.1128/mSystems.01017-20 PubMed DOI PMC

Pan Y., Birdsey R. A., Fang J., Houghton R., Kauppi P. E., Kurz W. A., et al. . (2011). A large and persistent carbon sink in the world's forests. Science 333, 988–993. 10.1126/science.1201609 PubMed DOI

Philpott T. J., Prescott C. E., Chapman W. K., Grayston S. J. (2014). Nitrogen translocation and accumulation by a cord-forming fungus (Hypholoma fasciculare) into simulated woody debris. For. Ecol. Manage. 315, 121–128. 10.1016/j.foreco.2013.12.034 DOI

Prestat E., David M. M., Hultman J., Taş N., Lamendella R., Dvornik J., et al. . (2014). FOAM (Functional Ontology Assignments for Metagenomes): a Hidden Markov Model (HMM) database with environmental focus. Nucleic Acids Res. 42:e145. 10.1093/nar/gku702 PubMed DOI PMC

Price M. N., Dehal P. S., Arkin A. P. (2010). FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. 10.1371/journal.pone.0009490 PubMed DOI PMC

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., et al. . (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596. 10.1093/nar/gks1219 PubMed DOI PMC

R Core Team (2020). R: A Language and Environment for Statistical Computing. Available online at: http://www.r-project.org/ (accessed June 22, 2020).

Rayner A. D., Boddy L. (1988). Fungal Decomposition of Wood. Its Biology and Ecology. Hoboken, NJ: John Wiley and Sons Ltd.

Rinne K. T., Rajala T., Peltoniemi K., Chen J., Smolander A., Mäkipää R. (2016). Accumulation rates and sources of external nitrogen in decaying wood in a Norway spruce dominated forest. Funct. Ecol. 31, 530–541. 10.1111/1365-2435.12734 DOI

Rinta-Kanto J. M., Sinkko H., Rajala T., Al-Soud W. A., Sørensen S. J., Tamminen M. V., et al. . (2016). Natural decay process affects the abundance and community structure of Bacteria and Archaea in Picea abies logs. FEMS Microbiol. Ecol. 92:fiw087. 10.1093/femsec/fiw087 PubMed DOI

Rognes T., Flouri T., Nichols B., Quince C., Mahé F. (2016). VSEARCH: a versatile open source tool for metagenomics. PeerJ. 4:e2584. 10.7717/peerj.2584 PubMed DOI PMC

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

Šamonil P., Schaetzl R. J., Valtera M., Goliáš V., Baldrian P., Vašíčková I., et al. . (2013). Crossdating of disturbances by tree uprooting: can treethrow microtopography persist for 6000 years? For. Ecol. Manage. 307, 123–135. 10.1016/j.foreco.2013.06.045 DOI

Seemann T. (2014). Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069. 10.1093/bioinformatics/btu153 PubMed DOI

Seidler R. J., Aho P. E., Raju P. N., Evans H. J. (1972). Nitrogen fixation by bacterial isolates from decay in living white fir trees [Abies concolor (Gord. and Glend.) Lindl.]. J. Gen. Microbiol. 73, 413–416. 10.1099/00221287-73-2-413 DOI

Shaiber A., Eren A. M. (2019). Composite metagenome-assembled genomes reduce the quality of public genome repositories. mBio 10, e00725–e00719. 10.1128/mBio.00725-19 PubMed DOI PMC

Spano S. D., Jurgensen M. F., Larsen M. J., Harvey A. E. (1982). Nitrogen-fixing bacteria in Douglas-fir residue decayed by Fomitopsis pinicola. Plant Soil 68, 117–123. 10.1007/BF02374731 DOI

Starke R., Morais D., Větrovský T., Mondéjar R. L., Baldrian P., Brabcová V. (2020). Feeding on fungi: genomic and proteomic analysis of the enzymatic machinery of bacteria decomposing fungal biomass. Environ. Microbiol. 22, 4604–4619. 10.1111/1462-2920.15183 PubMed DOI

Tange O. (2018). GNU Parallel. Frederiksberg: The USENIX Magazine.

Tláskal V., Brabcová V., Větrovský T., Jomura M., López-Mondéjar R., Monteiro M. O. L., et al. . (2021a). Complementary roles of wood-inhabiting fungi and bacteria facilitate deadwood decomposition. mSystems 6, e01078–e01020. 10.1128/mSystems.01078-20 PubMed DOI PMC

Tláskal V., Žifčáková L., Pylro V. S., Baldrian P. (2021b). Ecological divergence within the enterobacterial genus Sodalis: from insect symbionts to inhabitants of decomposing deadwood. Front. Microbiol. 12:668644. 10.3389/fmicb.2021.668644 PubMed DOI PMC

Tláskal V., Zrustová P., Vrška T., Baldrian P. (2017). Bacteria associated with decomposing dead wood in a natural temperate forest. FEMS Microbiol. Ecol. 93:fix157. 10.1093/femsec/fix157 PubMed DOI

Uroz S., Courty P. E., Pierrat J. C., Peter M., Buée M., Turpault M. P., et al. . (2013). Functional profiling and distribution of the forest soil bacterial communities along the soil mycorrhizosphere continuum. Microb. Ecol. 66, 404–415. 10.1007/s00248-013-0199-y PubMed DOI

Valášková V., de Boer W., Gunnewiek P. J. A. K., Pospíšek M., Baldrian P. (2009). Phylogenetic composition and properties of bacteria coexisting with the fungus Hypholoma fasciculare in decaying wood. ISME J. 3, 1218–1221. 10.1038/ismej.2009.64 PubMed DOI

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

Vorob'ev A. V., de Boer W., Folman L. B., Bodelier P. L. E., Doronina N. V., Suzina N. E., et al. . (2009). Methylovirgula ligni gen. nov., sp. nov., an obligately acidophilic, facultatively methylotrophic bacterium with a highly divergent mxaF gene. Int. J. Syst. Evol. Microbiol. 59, 2538–2545. 10.1099/ijs.0.010074-0 PubMed DOI

Walker B. J., Abeel T., Shea T., Priest M., Abouelliel A., Sakthikumar S., et al. . (2014). Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly omprovement. PLoS ONE 9:e112963. 10.1371/journal.pone.0112963 PubMed DOI PMC

Weedon J. T., Cornwell W. K., Cornelissen J. H. C., Zanne A. E., Wirth C., Coomes D. A. (2009). Global meta-analysis of wood decomposition rates: a role for trait variation among tree species? Ecol. Lett. 12, 45–56. 10.1111/j.1461-0248.2008.01259.x PubMed DOI

Wick R. R., Judd L. M., Gorrie C. L., Holt K. E. (2017). Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13:e1005595. 10.1371/journal.pcbi.1005595 PubMed DOI PMC

Wickham H., Averick M., Bryan J., Chang W., Mcgowan L. D. A., François R., et al. . (2019). Welcome to the Tidyverse. J. Open Source Softw. 4:1686. 10.21105/joss.01686 DOI

Wright E. S. (2016). Using DECIPHER v2.0 to analyze big biological sequence data in R. R J. 8, 352–359. 10.32614/RJ-2016-025 DOI

Zhang H., Yohe T., Huang L., Entwistle S., Wu P., Yang Z., et al. . (2018). dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 46, W95–W101. 10.1093/nar/gky418 PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...