Microorganisms dominate all ecosystems on Earth and play a key role in the turnover of organic matter. By producing enzymes, they degrade complex carbohydrates, facilitating the recycling of nutrients and controlling the carbon cycle. Despite their importance, our knowledge regarding microbial carbohydrate utilization has been limited to genome-sequenced taxa and thus heavily biased to specific groups and environments. Here, we used the Genomes from Earth's Microbiomes (GEM) catalog to describe the carbohydrate utilization potential in >7000 bacterial and archaeal taxa originating from a range of terrestrial, marine and host-associated habitats. We show that the production of carbohydrate-active enzymes (CAZymes) is phylogenetically conserved and varies significantly among microbial phyla. High numbers of carbohydrate-active enzymes were recorded in phyla known for their versatile use of carbohydrates, such as Firmicutes, Fibrobacterota, and Armatimonadota, but also phyla without cultured representatives whose carbohydrate utilization potential was so far unknown, such as KSB1, Hydrogenedentota, Sumerlaeota, and UBP3. Carbohydrate utilization potential reflected the specificity of various habitats: the richest complements of CAZymes were observed in MAGs of plant microbiomes, indicating the structural complexity of plant biopolymers. IMPORTANCE This study expanded our knowledge of the phylogenetic distribution of carbohydrate-active enzymes across prokaryotic tree of life, including new phyla where the carbohydrate-active enzymes composition have not been described until now and demonstrated the potential for carbohydrate utilization of numerous yet uncultured phyla. Profiles of carbohydrate-active enzymes are largely habitat-specific and reflect local carbohydrate availability by selecting taxa with appropriate complements of these enzymes. This information should aid in the prediction of functions in microbiomes of known taxonomic composition and helps to identify key components of habitat-specific carbohydrate pools. In addition, these findings have a high relevance for the understanding of carbohydrate utilization and carbon cycling in the environment, the process that is closely link to the carbon storage potential of Earth habitats and the production of greenhouse gasses.

CEBAS CSIC Department of Soil and Water Conservation Campus Universitario de Espinardo Murcia Spain

Department of Environmental Microbiology UFZ Helmholtz Centre for Environmental Research Leipzig Germany

Laboratory of Environmental Microbiology Institute of Microbiology of the Czech Academy of Sciences Prague Czech Republic

Zobrazit více v PubMed

Ogle K. 2018. Microbes weaken soil carbon sink. Nature 560:32–33. doi:10.1038/d41586-018-05842-2. PubMed DOI

Cavicchioli R, Ripple WJ, Timmis KN, Azam F, Bakken LR, Baylis M, Behrenfeld MJ, Boetius A, Boyd PW, Classen AT, Crowther TW, Danovaro R, Foreman CM, Huisman J, Hutchins DA, Jansson JK, Karl DM, Koskella B, Mark Welch DB, Martiny JBH, Moran MA, Orphan VJ, Reay DS, Remais JV, Rich VI, Singh BK, Stein LY, Stewart FJ, Sullivan MB, van Oppen MJH, Weaver SC, Webb EA, Webster NS. 2019. Scientists' warning to humanity: microorganisms and climate change. Nat Rev Microbiol 17:569–586. doi:10.1038/s41579-019-0222-5. PubMed DOI PMC

Jansson JK, Hofmockel KS. 2020. Soil microbiomes and climate change. Nat Rev Microbiol 18:35–46. doi:10.1038/s41579-019-0265-7. PubMed DOI

Arnosti C. 2011. Microbial extracellular enzymes and the marine carbon cycle. Annu Rev Mar Sci 3:401–425. doi:10.1146/annurev-marine-120709-142731. PubMed DOI

El Kaoutari A, Armougom F, Gordon JI, Raoult D, Henrissat B. 2013. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol 11:497–504. doi:10.1038/nrmicro3050. PubMed DOI

Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–495. doi:10.1093/nar/gkt1178. PubMed DOI PMC

Levasseur A, Drula E, Lombard V, Coutinho PM, Henrissat B. 2013. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41. doi:10.1186/1754-6834-6-41. PubMed DOI PMC

Horn SJ, Vaaje-Kolstad G, Westereng B, Eijsink VG. 2012. Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:45. doi:10.1186/1754-6834-5-45. PubMed DOI PMC

Thompson LR, Sanders JG, McDonald D, Amir A, Ladau J, Locey KJ, Prill RJ, Tripathi A, Gibbons SM, Ackermann G, Navas-Molina JA, Janssen S, Kopylova E, Vazquez-Baeza Y, Gonzalez A, Morton JT, Mirarab S, Zech Xu S, Jiang L, Haroon MF, Kanbar J, Zhu Q, Jin Song S, Kosciolek T, Bokulich NA, Lefler J, Brislawn CJ, Humphrey G, Owens SM, Hampton-Marcell J, Berg-Lyons D, McKenzie V, Fierer N, Fuhrman JA, Clauset A, Stevens RL, Shade A, Pollard KS, Goodwin KD, Jansson JK, Gilbert JA, Knight RC, Earth Microbiome Project Consortium . 2017. Earth Microbiome Project, a communal catalogue reveals Earth's multiscale microbial diversity. Nature 551:457–463. doi:10.1038/nature24621. PubMed DOI PMC

Flemming HC, Wuertz S. 2019. Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol 17:247–260. doi:10.1038/s41579-019-0158-9. PubMed DOI

Zimmerman AE, Martiny AC, Allison SD. 2013. Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. ISME J 7:1187–1199. doi:10.1038/ismej.2012.176. PubMed DOI PMC

Berlemont R, Martiny AC. 2015. Genomic potential for polysaccharides deconstruction in bacteria. Appl Environ Microbiol 81:1513–1519. doi:10.1128/AEM.03718-14. PubMed DOI PMC

Berlemont R, Martiny AC. 2016. Glycoside hydrolases across environmental microbial communities. PLoS Comput Biol 12:e1005300. doi:10.1371/journal.pcbi.1005300. PubMed DOI PMC

Martiny AC. 2019. High proportions of bacteria are culturable across major biomes. ISME J 13:2125–2128. doi:10.1038/s41396-019-0410-3. PubMed DOI PMC

Steen AD, Crits-Christoph A, Carini P, DeAngelis KM, Fierer N, Lloyd KG, Cameron Thrash J. 2019. High proportions of bacteria and archaea across most biomes remain uncultured. ISME J 13:3126–3130. doi:10.1038/s41396-019-0484-y. PubMed DOI PMC

Parks DH, Rinke C, Chuvochina M, Chaumeil PA, Woodcroft BJ, Evans PN, Hugenholtz P, Tyson GW. 2017. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2:1533–1542. doi:10.1038/s41564-017-0012-7. PubMed DOI

Adam PS, Borrel G, Brochier-Armanet C, Gribaldo S. 2017. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J 11:2407–2425. doi:10.1038/ismej.2017.122. PubMed DOI PMC

Castelle CJ, Brown CT, Anantharaman K, Probst AJ, Huang RH, Banfield JF. 2018. Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations. Nat Rev Microbiol 16:629–645. doi:10.1038/s41579-018-0076-2. PubMed DOI

Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N, Schulz F, Wu D, Paez-Espino D, Chen IM, Huntemann M, Palaniappan K, Ladau J, Mukherjee S, Reddy TBK, Nielsen T, Kirton E, Faria JP, Edirisinghe JN, Henry CS, Jungbluth SP, Chivian D, Dehal P, Wood-Charlson EM, Arkin AP, Tringe SG, Visel A, Consortium IMD, Woyke T, Mouncey NJ, Ivanova NN, Kyrpides NC, Eloe-Fadrosh EA, IMG/M Data Consortium . 2021. A genomic catalog of Earth's microbiomes. Nat Biotechnol 39:499–509. doi:10.1038/s41587-020-0718-6. PubMed DOI PMC

Peng X, Wilken SE, Lankiewicz TS, Gilmore SP, Brown JL, Henske JK, Swift CL, Salamov A, Barry K, Grigoriev IV, Theodorou MK, Valentine DL, O'Malley MA. 2021. Genomic and functional analyses of fungal and bacterial consortia that enable lignocellulose breakdown in goat gut microbiomes. Nat Microbiol 6:499–511. doi:10.1038/s41564-020-00861-0. PubMed DOI PMC

Woodcroft BJ, Singleton CM, Boyd JA, Evans PN, Emerson JB, Zayed AAF, Hoelzle RD, Lamberton TO, McCalley CK, Hodgkins SB, Wilson RM, Purvine SO, Nicora CD, Li C, Frolking S, Chanton JP, Crill PM, Saleska SR, Rich VI, Tyson GW. 2018. Genome-centric view of carbon processing in thawing permafrost. Nature 560:49–54. doi:10.1038/s41586-018-0338-1. PubMed DOI

Lopez-Mondejar R, Algora C, Baldrian P. 2019. Lignocellulolytic systems of soil bacteria: a vast and diverse toolbox for biotechnological conversion processes. Biotechnol Adv 37:107374. doi:10.1016/j.biotechadv.2019.03.013. PubMed DOI

Doud DFR, Bowers RM, Schulz F, De Raad M, Deng K, Tarver A, Glasgow E, Vander Meulen K, Fox B, Deutsch S, Yoshikuni Y, Northen T, Hedlund BP, Singer SW, Ivanova N, Woyke T. 2020. Function-driven single-cell genomics uncovers cellulose-degrading bacteria from the rare biosphere. ISME J 14:659–675. doi:10.1038/s41396-019-0557-y. PubMed DOI PMC

Graham ED, Tully BJ. 2021. Marine Dadabacteria exhibit genome streamlining and phototrophy-driven niche partitioning. ISME J 15:1248–1256. doi:10.1038/s41396-020-00834-5. PubMed DOI PMC

Zhao Z, Baltar F, Herndl GJ. 2020. Linking extracellular enzymes to phylogeny indicates a predominantly particle-associated lifestyle of deep-sea prokaryotes. Sci Adv 6:eaaz4354. doi:10.1126/sciadv.aaz4354. PubMed DOI PMC

Martiny AC, Treseder K, Pusch G. 2013. Phylogenetic conservatism of functional traits in microorganisms. ISME J 7:830–838. doi:10.1038/ismej.2012.160. PubMed DOI PMC

Royalty TM, Steen AD. 2019. Quantitatively partitioning microbial genomic traits among taxonomic ranks across the microbial tree of life. mSphere 4:e00446-19. doi:10.1128/mSphere.00637-19. PubMed DOI PMC

Martiny JB, Jones SE, Lennon JT, Martiny AC. 2015. Microbiomes in light of traits: a phylogenetic perspective. Science 350:aac9323. doi:10.1126/science.aac9323. PubMed DOI

Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. doi:10.1038/nbt.2676. PubMed DOI PMC

Sun ZZ, Ji BW, Zheng N, Wang M, Cao Y, Wan L, Li S, Rong JC, He HL, Chen XL, Zhang YZ, Xie BB. 2021. Phylogenetic distribution of polysaccharide-degrading enzymes in marine bacteria. Front Microbiol 12:658620. doi:10.3389/fmicb.2021.658620. PubMed DOI PMC

Talamantes D, Biabini N, Dang H, Abdoun K, Berlemont R. 2016. Natural diversity of cellulases, xylanases, and chitinases in bacteria. Biotechnol Biofuels 9:133. doi:10.1186/s13068-016-0538-6. PubMed DOI PMC

Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD. 2007. Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807. doi:10.1126/science.1137016. PubMed DOI

Luis AS, Martens EC. 2018. Interrogating gut bacterial genomes for discovery of novel carbohydrate degrading enzymes. Curr Opin Chem Biol 47:126–133. doi:10.1016/j.cbpa.2018.09.012. PubMed DOI

Hess M, Sczyrba A, Egan R, Kim TW, Chokhawala H, Schroth G, Luo S, Clark DS, Chen F, Zhang T, Mackie RI, Pennacchio LA, Tringe SG, Visel A, Woyke T, Wang Z, Rubin EM. 2011. Metagenomic discovery of biomass-degrading genes and genomes from cow rumen. Science 331:463–467. doi:10.1126/science.1200387. PubMed DOI

Becker S, Tebben J, Coffinet S, Wiltshire K, Iversen MH, Harder T, Hinrichs KU, Hehemann JH. 2020. Laminarin is a major molecule in the marine carbon cycle. Proc Natl Acad Sci USA 117:6599–6607. doi:10.1073/pnas.1917001117. PubMed DOI PMC

Žifčáková L, Větrovský T, Lombard V, Henrissat B, Howe A, Baldrian P. 2017. Feed in summer, rest in winter: microbial carbon utilization in forest topsoil. Microbiome 5:122. doi:10.1186/s40168-017-0340-0. PubMed DOI PMC

Battin TJ, Luyssaert S, Kaplan LA, Aufdenkampe AK, Richter A, Tranvik LJ. 2009. The boundless carbon cycle. Nature Geosci 2:598–600. doi:10.1038/ngeo618. DOI

Wehrli B. 2013. Conduits of the carbon cycle. Nature 503:346–347. doi:10.1038/503346a. PubMed DOI

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

Huang L, Zhang H, Wu P, Entwistle S, Li X, Yohe T, Yi H, Yang Z, Yin Y. 2018. dbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation. Nucleic Acids Res 46:D516–D521. doi:10.1093/nar/gkx894. PubMed DOI PMC

Eddy SR. 2011. Accelerated Profile HMM Searches. PLoS Comput Biol 7:e1002195. doi:10.1371/journal.pcbi.1002195. PubMed DOI PMC

Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. 2007. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108. doi:10.1093/nar/gkm160. PubMed DOI PMC

Katoh K, Rozewicki J, Yamada KD. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. doi:10.1093/bib/bbx108. PubMed DOI PMC

Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. doi:10.1093/molbev/msw054. PubMed DOI PMC

Oksanen J, Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin P, O'Hara R, Simpson G, Solymos P, Stevens M, Szoecs E, Wagner H. 2018. Vegan: community ecology package. R package version 2.5–2. https://cran.r-project.org/web/packages/vegan/index.html.

RCoreTeam. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing; [https://www.R-project.org/].

Teufel T, Almagro Armenteros JJ, Johansen AR, Gíslason MH, Pihl SI, Tsirigos KD, Winther O, Brunak S, Von Heijne G, Nielsen H. 2022. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol 40:1023–1025. doi:10.1038/s41587-021-01156-3. PubMed DOI PMC

Keck F, Rimet F, Bouchez A, Franc A. 2016. phylosignal: an R package to measure, test, and explore the phylogenetic signal. Ecol Evol 6:2774–2780. doi:10.1002/ece3.2051. PubMed DOI PMC

Abouheif E. 1999. A method for testing the assumption of phylogenetic independence in comparative data. Evol Ecol Res 1:895–909.

Louca S, Doebeli M. 2018. Efficient comparative phylogenetics on large trees. Bioinformatics 34:1053–1055. doi:10.1093/bioinformatics/btx701. PubMed DOI

Racine JS. 2012. RStudio: a Platform-Independent IDE for R and Sweave. J Appl Econ 27:167–172. doi:10.1002/jae.1278. DOI

Wickham H, Averick M, Bryan J, Chang W, McGowan LD, François R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen TL, Miller E, Bache SM, Müller K, Ooms J, Robinson D, Seidel DP, Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H. 2019. Welcome to the tidyverse. JOSS 4:1686. doi:10.21105/joss.01686. DOI

Letunic I, Bork P. 2019. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47:W256–W259. doi:10.1093/nar/gkz239. PubMed DOI PMC

Long-read sequencing sheds light on key bacteria contributing to deadwood decomposition processes

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.16435581