Abstract
The Acidobacteria phylum is a very abundant group (20–30% of microbial communities in soil ecosystems); however, little is known about these microorganisms and their ability to degrade the biomass and lignocellulose due to the difficulty of culturing them. We, therefore, bioinformatically studied the content of lignocellulolytic enzymes (total and predicted secreted enzymes) and secreted peptidases in an in silico library containing 41 Acidobacteria genomes. The results showed a high abundance and diversity of total and secreted Carbohydrate-Active enzymes (cazyme) families among the Acidobacteria compared to known previous degraders. Indeed, the relative abundance of cazymes in some genomes represented more than 6% of the gene coding proteins with at least 300 cazymes. The same observation was made with the predicted secreted peptidases with several families of secreted peptidases, which represented at least 1.5% of the gene coding proteins in several genomes. These results allowed us to highlight the lignocellulolytic potential of the Acidobacteria phylum in the degradation of lignocellulosic biomass, which could explain its high abundance in the environment.
Similar content being viewed by others
References
Almagro Armenteros JJ, Tsirigos KD, Sønderby CK et al (2019) SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 37:420–423
Aragunde H, Biarnés X, Planas A (2018) Substrate recognition and specificity of chitin deacetylases and related family 4 carbohydrate esterases. Int J Mol Sci 19:412
Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on Earth. Proc Natl Acad Sci 115:6506–6511
Bei Q, Moser G, Müller C, Liesack W (2021) Seasonality affects function and complexity but not diversity of the rhizosphere microbiome in European temperate grassland. Sci Total Environ 784:147036
Bengtsson O, Arntzen MØ, Mathiesen G et al (2016) A novel proteomics sample preparation method for secretome analysis of Hypocrea jecorina growing on insoluble substrates. J Proteomics 131:104–112
Besaury L, Rémond C (2022) Culturable and metagenomic approaches of wheat bran and wheat straw phyllosphere’s highlight new lignocellulolytic microorganisms. Lett Appl Microbiol 74:840–850
Biswas R, Uellendahl H, Ahring BK (2015) Wet explosion: a universal and efficient pretreatment process for lignocellulosic biorefineries. BioEnergy Research 8:1101–1116
Blondel VD, Guillaume J-L, Lambiotte R, Lefebvre E (2008) Fast unfolding of communities in large networks. J Stat Mech: Theory Exp 2008:P10008
Bobay L-M, Ochman H (2017) The evolution of bacterial genome architecture. Front Genet 8:72
Brás JL, Cartmell A, Carvalho ALM et al (2011) Structural insights into a unique cellulase fold and mechanism of cellulose hydrolysis. Proc Natl Acad Sci 108:5237–5242
Brumm P, Hermanson S, Hochstein B et al (2011) Mining Dictyoglomus turgidum for enzymatically active carbohydrases. Appl Biochem Biotechnol 163:205–214
Bury D, Dahmane I, Derouaux A et al (2015) Positive cooperativity between acceptor and donor sites of the peptidoglycan glycosyltransferase. Biochem Pharmacol 93:141–150
Cantarel BL, Coutinho PM, Rancurel C et al (2008) The carbohydrate-active enzymes database (cazy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238
Cassarini M, Besaury L, Rémond C (2021) Valorisation of wheat bran to produce natural pigments using selected microorganisms. J Biotechnol 339:81–92
Cassarini M, Crônier D, Besaury L, Rémond C (2022) Protein-rich agro-industrial co-products are key substrates for growth of Chromobacterium vaccinii and its violacein bioproduction. Waste Biomass Valoriz 13(11):4459–4468
Chakraborty J, Suzuki-Minakuchi C, Tomita T et al (2021) A novel gene cluster is involved in the degradation of lignin-derived monoaromatics in Thermus oshimai JL-2. Appl Environ Microbiol 87:e01589-e1620
Costa OY (2020) Ecological functions and environmental fate of exopolymers of Acidobacteria. PhD Thesis
De Chaves MG, Silva GGZ, Rossetto R et al (2019) Acidobacteria subgroups and their metabolic potential for carbon degradation in sugarcane soil amended with vinasse and nitrogen fertilizers. Front Microbiol 10:1680
Dedysh SN, Damsté JSS (2018) Acidobacteria. eLS. Wiley, pp 1–10
Dedysh SN, Yilmaz P (2018) Refining the taxonomic structure of the phylum Acidobacteria. Int J Syst Evol Microbiol 68(12):3796–3806
Detain J, Rémond C, Rodrigues CM et al (2022) Co-elicitation of lignocelluloytic enzymatic activities and metabolites production in an Aspergillus-Streptomyces co-culture during lignocellulose fractionation. Curr Res Microb Sci 3:100108
Diamond S, Andeer PF, Li Z et al (2019) Mediterranean grassland soil C-N compound turnover is dependent on rainfall and depth, and is mediated by genomically divergent microorganisms. Nat Microbiol 4:1356–1367
Dong Z, Yang S, Lee BH (2021) Bioinformatic mapping of a more precise Aspergillus niger degradome. Sci Rep 11:1–21
Espersen R, Huang Y, Falco FC et al (2021) Exceptionally rich keratinolytic enzyme profile found in the rare actinomycetes Amycolatopsis keratiniphila D2T. Appl Microbiol Biotechnol 105:8129–8138
Gavande PV, Basak A, Sen S et al (2021) Functional characterization of thermotolerant microbial consortium for lignocellulolytic enzymes with central role of Firmicutes in rice straw depolymerization. Sci Rep 11:1–13
Greening C, Carere CR, Rushton-Green R et al (2015) Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging. Proc Natl Acad Sci 112:10497–10502
Guerriero G, Hausman J-F, Strauss J et al (2016) Lignocellulosic biomass: biosynthesis, degradation, and industrial utilization. Eng Life Sci 16:1–16
Häkkinen M, Arvas M, Oja M et al (2012) Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb Cell Fact 11:1–26
Hale L, Feng W, Yin H et al (2019) Tundra microbial community taxa and traits predict decomposition parameters of stable, old soil organic carbon. ISME J 13:2901–2915
Herbaut M, Zoghlami A, Habrant A et al (2018) Multimodal analysis of pretreated biomass species highlights generic markers of lignocellulose recalcitrance. Biotechnol Biofuels 11:1–17
Jacquiod S, Franqueville L, Cecillon S et al (2013) Soil bacterial community shifts after chitin enrichment: an integrative metagenomic approach. PLoS One 8:e79699
Kalam S, Basu A, Ahmad I et al (2020) Recent understanding of soil acidobacteria and their ecological significance: a critical review. Front Microbiol 11:580024
Karnaouri A, Topakas E, Paschos T et al (2013) Cloning, expression and characterization of an ethanol tolerant GH3 β-glucosidase from Myceliophthora thermophila. PeerJ 1:e46
Karp PD, Riley M, Paley SM, Pellegrini-Toole A (2002) The metacyc database. Nucleic Acids Res 30:59–61
Kielak AM, Barreto CC, Kowalchuk GA et al (2016) The ecology of Acidobacteria: moving beyond genes and genomes. Front Microbiol 7:744
Koupaie EH, Dahadha S, Lakeh AB et al (2019) Enzymatic pretreatment of lignocellulosic biomass for enhanced biomethane production-a review. J Environ Manage 233:774–784
Krogh A, Larsson B, Von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580
Lacerda Júnior GV, Noronha MF, de Sousa STP et al (2017) Potential of semiarid soil from Caatinga biome as a novel source for mining lignocellulose-degrading enzymes. FEMS Microbiol Ecol 93(2)
Lladó S, Žifčáková L, Větrovský T et al (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
Lu J, Yang Z, Xu W et al (2019) Enrichment of thermophilic and mesophilic microbial consortia for efficient degradation of corn stalk. J Environ Sci 78:118–126
Mai-Gisondi G, Maaheimo H, Chong S-L et al (2017) Functional comparison of versatile carbohydrate esterases from families CE1, CE6 and CE16 on acetyl-4-O-methylglucuronoxylan and acetyl-galactoglucomannan. Biochim Biophys Acta Gen Subj 1861:2398–2405
Nakamura AM, Nascimento AS, Polikarpov I (2017) Structural diversity of carbohydrate esterases. Biotechnol Res Innov 1:35–51
Nam S, Alday JG, Kim M et al (2021) The relationships of present vegetation, bacteria, and soil properties with soil organic matter characteristics in moist acidic tundra in Alaska. Sci Total Environ 772:145386
Naumoff DG (2016) GH10 family of glycoside hydrolases: structure and evolutionary connections. Mol Biol 50:132–140
Navarrete AA, Venturini AM, Meyer KM et al (2015) Differential response of Acidobacteria subgroups to forest-to-pasture conversion and their biogeographic patterns in the western Brazilian Amazon. Front Microbiol 6:1443
Nekiunaite L, Arntzen MØ, Svensson B et al (2016) Lytic polysaccharide monooxygenases and other oxidative enzymes are abundantly secreted by Aspergillus nidulans grown on different starches. Biotechnol Biofuels 9:1–16
Ondov BD, Treangen TJ, Melsted P et al (2016) Mash: fast genome and metagenome distance estimation using MinHash. Genome Biol 17:1–14
Pankratov TA, Serkebaeva YM, Kulichevskaya IS et al (2008) Substrate-induced growth and isolation of Acidobacteria from acidic Sphagnum peat. ISME J 2:551–560
Patra AK, Yu Z (2022) Genomic insights into the distribution of peptidases and proteolytic capacity among Prevotella and Paraprevotella species. Microbiol Spectr 10:e02185-e2221
Petit E, Coppi MV, Hayes JC et al (2015) Genome and transcriptome of Clostridium phytofermentans, catalyst for the direct conversion of plant feedstocks to fuels. PLoS One 10:e0118285
Piccinni FE, Ontañon OM, Ghio S et al (2019) Secretome profile of Cellulomonas sp. B6 growing on lignocellulosic substrates. J Appl Microbiol 126:811–825
Poria V, Saini JK, Singh S et al (2020) Arabinofuranosidases: characteristics, microbial production, and potential in waste valorization and industrial applications. Biores Technol 304:123019
Rawat SR, Männistö MK, Bromberg Y, Häggblom MM (2012) Comparative genomic and physiological analysis provides insights into the role of Acidobacteria in organic carbon utilization in Arctic tundra soils. FEMS Microbiol Ecol 82:341–355
Rawlings ND, Barrett AJ, Bateman A (2010) MEROPS: the peptidase database. Nucleic Acids Res 38:D227–D233
Ricard G, McEwan NR, Dutilh BE et al (2006) Horizontal gene transfer from Bacteria to rumen ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC Genomics 7:1–13
Rodrigues GR, Pinto OHB, Schroeder LF et al (2020) Unraveling the xylanolytic potential of Acidobacteria bacterium AB60 from Cerrado soils. FEMS Microbiol Lett 367:fnaa149
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Strazzulli A, Cobucci-Ponzano B, Iacono R et al (2020) Discovery of hyperstable carbohydrate-active enzymes through metagenomics of extreme environments. FEBS J 287:1116–1137
Tolonen AC, Haas W, Chilaka AC et al (2011) Proteome-wide systems analysis of a cellulosic biofuel-producing microbe. Mol Syst Biol 7:461
Trent MS, Ribeiro AA, Lin S et al (2001) An inner membrane enzyme in salmonellaand escherichia coli that transfers 4-amino-4-deoxy-l-arabinose to Lipid A: INDUCTION IN POLYMYXIN-RESISTANT MUTANTS AND ROLE OF A NOVEL LIPID-LINKED DONOR* 210. J Biol Chem 276:43122–43131
Van Hees PA, Jones DL, Finlay R et al (2005) The carbon we do not see—the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13
Ward NL, Challacombe JF, Janssen PH et al (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056
Williams-Rhaesa AM, Awuku NK, Lipscomb GL et al (2018) Native xylose-inducible promoter expands the genetic tools for the biomass-degrading, extremely thermophilic bacterium Caldicellulosiruptor bescii. Extremophiles 22:629–638
Zhang K, Chen X, Schwarz WH, Li F (2014) Synergism of glycoside hydrolase secretomes from two thermophilic bacteria cocultivated on lignocellulose. Appl Environ Microbiol 80:2592–2601
Zheng Y, Maruoka M, Nanatani K et al (2021) High cellulolytic potential of the Ktedonobacteria lineage revealed by genome-wide analysis of Cazymes. J Biosci Bioeng 131:622–630
Zhoukun L, Wenwen Z, Lei Z et al (2019) Gene expression and biochemical characterization of a GH77 4-α-glucanotransferase CcGtase From Corallococcus sp. EGB Starch-Stärke 71:1800254
Acknowledgements
The Funding support for this work has been received from EC2CO INSU “Novacultmic” project.
Author information
Authors and Affiliations
Contributions
MC and LB: performed data analysis, genetic data interpretation, and wrote custom scripts and the manuscript, participated in the discussions on the overall and detailed study plan. LB designed the research project and supervised it. All authors discussed the results and commented on the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no confict of interest.
Consent for publication
Not applicable.
Additional information
Communicated by Martine Collart.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Coluccia, M., Besaury, L. Acidobacteria members harbour an abundant and diverse carbohydrate-active enzymes (cazyme) and secreted proteasome repertoire, key factors for potential efficient biomass degradation. Mol Genet Genomics 298, 1135–1154 (2023). https://doi.org/10.1007/s00438-023-02045-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-023-02045-x