Abstract
Our current understanding of enzymatic polysaccharide degradation has come from a huge number of in vitro studies with purified enzymes. While this vast body of work has been invaluable in identifying and characterizing novel mechanisms of action and engineering desirable traits into these enzymes, a comprehensive picture of how these enzymes work as part of a native in vivo system is less clear. Recently, several model bacteria have emerged with genetic systems that allow for a more nuanced study of carbohydrate active enzymes (CAZymes) and how their activity affects bacterial carbon metabolism. With these bacterial model systems, it is now possible to not only study a single nutrient system in isolation (i.e., carbohydrate degradation and carbon metabolism), but also how multiple systems are integrated. Given that most environmental polysaccharides are carbon rich but nitrogen poor (e.g., lignocellulose), the interplay between carbon and nitrogen metabolism in polysaccharide-degrading bacteria can now be studied in a physiologically relevant manner. Therefore, in this review, we have summarized what has been experimentally determined for CAZyme regulation, production, and export in relation to nitrogen metabolism for two Gram-positive (Caldicellulosiruptor bescii and Clostridium thermocellum) and two Gram-negative (Bacteroides thetaiotaomicron and Cellvibrio japonicus) polysaccharide-degrading bacteria. By comparing and contrasting these four bacteria, we have highlighted the shared and unique features of each, with a focus on in vivo studies, in regard to carbon and nitrogen assimilation. We conclude with what we believe are two important questions that can act as guideposts for future work to better understand the integration of carbon and nitrogen metabolism in polysaccharide-degrading bacteria.
Key points
• Regardless of CAZyme deployment system, the generation of a local pool of oligosaccharides is a common strategy among Gram-negative and Gram-positive polysaccharide degraders as a means to maximally recoup the energy expenditure of CAZyme production and export.
• Due to the nitrogen deficiency of insoluble polysaccharide-containing substrates, Gram-negative and Gram-positive polysaccharide degraders have a diverse set of strategies for supplementation and assimilation.
• Future work needs to precisely characterize the energetic expenditures of CAZyme deployment and bolster our understanding of how carbon and nitrogen metabolism are integrated in both Gram-negative and Gram-positive polysaccharide-degrading bacteria, as both of these will significantly influence a given bacterium’s suitability for biotechnology applications.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
Adams BL (2016) The next generation of synthetic biology chassis: moving synthetic biology from the laboratory to the field. ACS Synth Biol 5(12):1328–1330. https://doi.org/10.1021/acssynbio.6b00256
Akinosho H, Yee K, Close D, Ragauskas A (2014) The emergence of Clostridium thermocellum as a high utility candidate for consolidated bioprocessing applications. Front Chem 2:66. https://doi.org/10.3389/fchem.2014.00066
André I, Potocki-Véronèse G, Barbe S, Moulis C, Remaud-Siméon M (2014) CAZyme discovery and design for sweet dreams. Curr Opin Chem Biol 19:17–24. https://doi.org/10.1016/j.cbpa.2013.11.014
Artzi L, Bayer EA, Moraïs S (2016) Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides. Nat Rev Microbiol 15(2):83–95. https://doi.org/10.1038/nrmicro.2016.164
Bandi CK, Agrawal A, Chundawat SP (2020) Carbohydrate-active enzyme (CAZyme) enabled glycoengineering for a sweeter future. Curr Opin Biotechnol 66:283–291. https://doi.org/10.1016/j.copbio.2020.09.006
Bergkessel M, Bast DW, Newman DK (2016) The physiology of growth arrest: uniting molecular and environmental microbiology. Nat Rev Microbiol 14(9):549–62. https://doi.org/10.1038/nrmicro.2016.107
Berlemont R (2017) Distribution and diversity of enzymes for polysaccharide degradation in fungi. Sci Rep 7(1):222. https://doi.org/10.1038/s41598-017-00258-w
Blake AD, Beri NR, Guttman HS, Cheng R, Gardner JG (2018) The complex physiology of Cellvibrio japonicus xylan degradation relies on a single cytoplasmic β-xylosidase for xylo-oligosaccharide utilization. Mol Microbiol 107(5):610–622. https://doi.org/10.1111/mmi.13903
Blumer-Schuette SE, Zurawski JV, Conway JM, Khatibi P, Lewis DL, Li Q, Chiang VL, Kelly RM (2017) Caldicellulosiruptor saccharolyticus transcriptomes reveal consequences of chemical pretreatment and genetic modification of lignocellulose. Microb Biotechnol 10(6):1546–1557. https://doi.org/10.1111/1751-7915.12494
Bolam DN, van den Berg B (2018) TonB-dependent transport by the gut microbiota: novel aspects of an old problem. Curr Opin Struct Biol 51:35–43. https://doi.org/10.1016/j.sbi.2018.03.001
Briggs JA, Grondin JM, Brumer H (2020) Communal living: glycan utilization by the human gut microbiota. Environ Microbiol 23(1):15–35. https://doi.org/10.1111/1462-2920.15317
Bruggeman FJ, Planqué R, Molenaar D, Teusink B (2020) Searching for principles of microbial physiology. FEMS Microbiol Rev 44(6):821–844. https://doi.org/10.1093/femsre/fuaa034
Bule P, Pires VM, Fontes CM, Alves VD (2018) Cellulosome assembly: paradigms are meant to be broken! Curr Opin Struct Biol 49:154–161. https://doi.org/10.1016/j.sbi.2018.03.012
Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2008) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37(Database issue):D233–8. https://doi.org/10.1093/nar/gkn663
Cezairliyan B, Ausubel FM (2017) Investment in secreted enzymes during nutrient-limited growth is utility dependent. Proc Natl Acad Sci U S A 114(37):E7796–E7802. https://doi.org/10.1073/pnas.1708580114
Chang C, Tesar C, Li X, Kim Y, Rodionov DA, Joachimiak A (2015) A novel transcriptional regulator of L-arabinose utilization in human gut bacteria. Nucleic Acids Res 43(21):10546–10559. https://doi.org/10.1093/nar/gkv1005
Chen Y, Nishihara A, Haruta S (2021) Nitrogen-fixing ability and nitrogen fixation-related genes of thermophilic fermentative bacteria in the genus Caldicellulosiruptor. Microbes Environ 36(2):ME21018. https://doi.org/10.1264/jsme2.ME21018
Chiang HC (2009) A hybrid two-component system in Bacteroides thetaiotaomicron that regulates nitrogen metabolism. Washington University
Choi J, Klingeman DM, Brown SD, Cox CD (2017) The LacI family protein GlyR3 co-regulates the celC operon and manB in Clostridium thermocellum. Biotechnol Biofuels 10:163. https://doi.org/10.1186/s13068-017-0849-2
Chung D, Cha M, Guss AM, Westpheling J (2014) Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii. Proc Natl Acad Sci U S A 111(24):8931–8936. https://doi.org/10.1073/pnas.1402210111
Claudia H (2010) Symbiosis in subterranean termites: a review of insights from molecular studies. Environ Entomol 39(2):378–388. https://doi.org/10.1603/EN09006
Comstock LE (2016) Small RNAs repress expression of polysaccharide utilization loci of gut Bacteroides species. J Bacteriol 198(18):2396–2398. https://doi.org/10.1128/JB.00514-16
Comstock LE, Coyne MJ (2003) Bacteroides thetaiotaomicron: a dynamic, niche-adapted human symbiont. BioEssays 25(10):926–929. https://doi.org/10.1002/bies.10350
Conway JM, Pierce WS, Le JH, Harper GW, Wright JH, Tucker AL, Zurawski JV, Lee LL, Blumer-Schuette SE, Kelly RM (2016a) Multidomain, surface layer-associated glycoside hydrolases contribute to plant polysaccharide degradation by Caldicellulosiruptor species. J Biol Chem 291(13):6732–6747. https://doi.org/10.1074/jbc.M115.707810
D’Elia JN, Salyers AA (1996) Effect of regulatory protein levels on utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 178(24):7180–7186. https://doi.org/10.1128/jb.178.24.7180-7186.1996
Dam P, Kataeva I, Yang SJ, Zhou F, Yin Y, Chou W, Poole FL, Westpheling J, Hettich R, Giannone R, Lewis DL, Kelly R, Gilbert HJ, Henrissat B, Xu Y, Adams MW (2011) Insights into plant biomass conversion from the genome of the anaerobic thermophilic bacterium Caldicellulosiruptor bescii DSM 6725. Nucleic Acids Res 39(8):3240–3254. https://doi.org/10.1093/nar/gkq1281
DeBoy RT, Mongodin EF, Fouts DE, Tailford LE, Khouri H, Emerson JB, Mohamoud Y, Watkins K, Henrissat B, Gilbert HJ, Nelson KE (2008) Insights into plant cell wall degradation from the genome sequence of the soil bacterium Cellvibrio japonicus. J Bacteriol 190(15):5455–5463. https://doi.org/10.1128/JB.01701-07
Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, Chivian D, Friedland GD, Huang KH, Keller K, Novichkov PS, Dubchak IL, Alm EJ, Arkin AP (2009) MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 38(Database issue):D396–400. https://doi.org/10.1093/nar/gkp919
Desvaux M, Khan A, Scott-Tucker A, Chaudhuri RR, Pallen MJ, Henderson IR (2005) Genomic analysis of the protein secretion systems in Clostridium acetobutylicum ATCC 824. Biochim Biophys Acta 1745(2):223–253. https://doi.org/10.1016/j.bbamcr.2005.04.006
Deutscher J (2008) The mechanisms of carbon catabolite repression in bacteria. Curr Opin Microbiol 11(2):87–93. https://doi.org/10.1016/j.mib.2008.02.007
Drescher K, Nadell CD, Stone HA, Wingreen NS, Bassler BL (2013) Solutions to the public goods dilemma in bacterial biofilms. Curr Biol 24(1):50–55. https://doi.org/10.1016/j.cub.2013.10.030
Dror TW, Morag E, Rolider A, Bayer EA, Lamed R, Shoham Y (2003a) Regulation of the cellulosomal CelS (cel48A) gene of Clostridium thermocellum is growth rate dependent. J Bacteriol 185(10):3042–3048. https://doi.org/10.1128/JB.185.10.3042-3048.2003
Dror TW, Rolider A, Bayer EA, Lamed R, Shoham Y (2003b) Regulation of expression of scaffoldin-related genes in Clostridium thermocellum. J Bacteriol 185(17):5109–5116. https://doi.org/10.1128/JB.185.17.5109-5116.2003
Ejby M, Fredslund F, Andersen JM, Vujičić Žagar A, Henriksen JR, Andersen TL, Svensson B, Slotboom DJ, Abou Hachem M (2016) An ATP binding cassette transporter mediates the uptake of α-(1,6)-linked dietary oligosaccharides in Bifidobacterium and correlates with competitive growth on these substrates. J Biol Chem 291(38):20220–20231. https://doi.org/10.1074/jbc.M116.746529
Elhenawy W, Debelyy MO, Feldman MF (2014) Preferential packing of acidic glycosidases and proteases into Bacteroides outer membrane vesicles. mBio 5(2):e00909–14. https://doi.org/10.1128/mBio.00909-14
Emami K, Nagy T, Fontes CM, Ferreira LM, Gilbert HJ (2002) Evidence for temporal regulation of the two Pseudomonas cellulosa xylanases belonging to glycoside hydrolase family 11. J Bacteriol 184(15):4124–4133. https://doi.org/10.1128/JB.184.15.4124-4133.2002
Emami K, Topakas E, Nagy T, Henshaw J, Jackson KA, Nelson KE, Mongodin EF, Murray JW, Lewis RJ, Gilbert HJ (2008) Regulation of the xylan-degrading apparatus of Cellvibrio japonicus by a novel two-component system. J Biol Chem 284(2):1086–1096. https://doi.org/10.1074/jbc.M805100200
Escalante A, Salinas Cervantes A, Gosset G, Bolívar F (2012) Current knowledge of the Escherichia coli phosphoenolpyruvate–carbohydrate phosphotransferase system: peculiarities of regulation and impact on growth and product formation. Appl Microbiol Biotechnol 94(6):1483–1494. https://doi.org/10.1007/s00253-012-4101-5
Feinberg L, Foden J, Barrett T, Davenport KW, Bruce D, Detter C, Tapia R, Han C, Lapidus A, Lucas S, Cheng JF, Pitluck S, Woyke T, Ivanova N, Mikhailova N, Land M, Hauser L, Argyros DA, Goodwin L, Hogsett D, Caiazza N (2011) Complete genome sequence of the cellulolytic thermophile Clostridium thermocellum DSM1313. J Bacteriol 193(11):2906–2907. https://doi.org/10.1128/JB.00322-11
Flint HJ, Bayer EA, Rincon MT, Lamed R, White BA (2008) Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat Rev Microbiol 6(2):121–131. https://doi.org/10.1038/nrmicro1817
Foley MH, Cockburn DW, Koropatkin NM (2016) The Sus operon: a model system for starch uptake by the human gut Bacteroidetes. Cell Mol Life Sci 73(14):2603–2617. https://doi.org/10.1007/s00018-016-2242-x
Fontes CM, Gilbert HJ (2010) Cellulosomes: highly efficient nanomachines designed to deconstruct plant cell wall complex carbohydrates. Annu Rev Biochem 79:655–681. https://doi.org/10.1146/annurev-biochem-091208-085603
Garcia CA, Gardner JG (2021) Bacterial α-diglucoside metabolism: perspectives and potential for biotechnology and biomedicine. Appl Microbiol Biotechnol 105(10):4033–4052. https://doi.org/10.1007/s00253-021-11322-x
Garcia CAN, J.A., Gardner, J.G. (2020) Trehalose degradation by Cellvibrio japonicus exhibits no functional redundancy and is solely dependent on the Tre37A enzyme. Appl Environ Microbiol 86(22):e01639-e1720. https://doi.org/10.1128/AEM.01639-20
Garcia-Garcera M, Rocha EPC (2020) Community diversity and habitat structure shape the repertoire of extracellular proteins in bacteria. Nat Commun 11(1):758. https://doi.org/10.1038/s41467-020-14572-x
Gardner JG (2016) Polysaccharide degradation systems of the saprophytic bacterium Cellvibrio japonicus. World J Microbiol Biotechnol 32(7):121. https://doi.org/10.1007/s11274-016-2068-6
Gardner JG, Keating DH (2010) Requirement of the type II secretion system for utilization of cellulosic substrates by Cellvibrio japonicus. Appl Environ Microbiol 76(15):5079–5087. https://doi.org/10.1128/AEM.00454-10
Gardner JG, Keating DH (2012) Genetic and functional genomic approaches for the study of plant cell wall degradation in Cellvibrio japonicus. Methods Enzymol 510:331–347. https://doi.org/10.1016/B978-0-12-415931-0.00018-5
Garron ML, Henrissat B (2019) The continuing expansion of CAZymes and their families. Curr Opin Chem Biol 53:82–87. https://doi.org/10.1016/j.cbpa.2019.08.004
Glowacki RWP, Martens EC (2020) If you eat it, or secrete it, they will grow: the expanding list of nutrients utilized by human gut bacteria. J Bacteriol. https://doi.org/10.1128/JB.00481-20
Gómez-Martín JM, Castaño-Díaz M, Cámara-Obregón A, Álvarez-Álvarez P, Folgueras-Díaz MB, Diez MA (2020) On the chemical composition and pyrolytic behavior of hybrid poplar energy crops from northern Spain. Energy Rep 6:764–769. https://doi.org/10.1016/j.egyr.2019.09.065
Green ERM, J. (2016) Bacterial secretion systems – an overview. Microbiol Spectr 4(1). https://doi.org/10.1128/microbiolspec.VMBF-0012-2015
Grinberg IR, Yaniv O, de Ora LO, Muñoz-Gutiérrez I, Hershko A, Livnah O, Bayer EA, Borovok I, Frolow F, Lamed R, Voronov-Goldman M (2019) Distinctive ligand-binding specificities of tandem PA14 biomass-sensory elements from Clostridium thermocellum and Clostridium clariflavum. Proteins 87(11):917–930. https://doi.org/10.1002/prot.25753
Guignard MSL, AR, Acquisti C, Eizaguirre C, Elser JJ, Hessen DO, Jeyasingh PD, Neiman M, Richardson AE, Soltis PS, Soltis DE, Stevens CJ, Trimmer M, Weider LJ, Woodward G, Leitch IJ (2017) Impacts of nitrogen and phosphorus: from genomes to natural ecosystems and agriculture. Front Ecol Evol 5(70). https://doi.org/10.3389/fevo.2017.00070
Gunka K, Commichau FM (2012) Control of glutamate homeostasis in Bacillus subtilis: a complex interplay between ammonium assimilation, glutamate biosynthesis and degradation. Mol Microbiol 85(2):213–224. https://doi.org/10.1111/j.1365-2958.2012.08105.x
Gunka K, Newman JA, Commichau FM, Herzberg C, Rodrigues C, Hewitt L, Lewis RJ, Stülke J (2010) Functional dissection of a trigger enzyme: mutations of the Bacillus subtilis glutamate dehydrogenase RocG that affect differentially its catalytic activity and regulatory properties. J Mol Biol 400(4):815–827. https://doi.org/10.1016/j.jmb.2010.05.055
Guthrie EP, Salyers AA (1986) Use of targeted insertional mutagenesis to determine whether chondroitin lyase II is essential for chondroitin sulfate utilization by Bacteroides thetaiotaomicron. J Bacteriol 166(3):966–971. https://doi.org/10.1128/jb.166.3.966-971.1986
Hanson AD, McCarty DR, Henry CS, Xian X, Joshi J, Patterson JA, García-García JD, Fleischmann SD, Tivendale ND, Millar AH (2021) The number of catalytic cycles in an enzyme’s lifetime and why it matters to metabolic engineering. Proc Natl Acad Sci U S A 118(13). https://doi.org/10.1073/pnas.2023348118
Hehemann JH, Correc G, Barbeyron T, Helbert W, Czjzek M, Michel G (2010) Transfer of carbohydrate-active enzymes from marine bacteria to Japanese gut microbiota. Nature 464(7290):908–912. https://doi.org/10.1038/nature08937
Hemsworth GR, Déjean G, Davies GJ, Brumer H (2016) Learning from microbial strategies for polysaccharide degradation. Biochem Soc Trans 44(1):94–108. https://doi.org/10.1042/BST20150180
Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8(1):15–25. https://doi.org/10.1038/nrmicro2259
Hooper LV, Xu J, Falk PG, Midtvedt T, Gordon JI (1999) A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc Natl Acad Sci U S A 96(17):9833–9838. https://doi.org/10.1073/pnas.96.17.9833
Horlamus F, Wittgens A, Noll P, Michler J, Müller I, Weggenmann F, Oellig C, Rosenau F, Henkel M, Hausmann R (2019) One-step bioconversion of hemicellulose polymers to rhamnolipids with Cellvibrio japonicus: a proof-of-concept for a potential host strain in future bioeconomy. GCB Bioenergy 11(1):260–268. https://doi.org/10.1111/gcbb.12542
Huergo LF, Chandra G, Merrick M (2012) P(II) signal transduction proteins: nitrogen regulation and beyond. FEMS Microbiol Rev 37(2):251–283. https://doi.org/10.1111/j.1574-6976.2012.00351.x
Huergo LF, Dixon R (2015) The emergence of 2-Oxoglutarate as a master regulator metabolite. Microbiol Mol Biol Rev 79(4):419–435. https://doi.org/10.1128/MMBR.00038-15
Iakiviak M (2017) Analysis of the ammonium assimilation pathways of the human colonic bacterium. University of Illinois at Urbana-Champaign, Bacteroides thetaiotaomicron
Igai K, Itakura M, Nishijima S, Tsurumaru H, Suda W, Tsutaya T, Tomitsuka E, Tadokoro K, Baba J, Odani S, Natsuhara K, Morita A, Yoneda M, Greenhill AR, Horwood PF, Inoue J-i, Ohkuma M, Hongoh Y, Yamamoto T, Siba PM, Hattori M, Minamisawa K, Umezaki M (2016) Nitrogen fixation and nifH diversity in human gut microbiota. Sci Rep 6(1):31942. https://doi.org/10.1038/srep31942
Jones DR, Smith MB, McLean R, Grondin JM, Amundsen CR, Inglis GD, Selinger B, Abbott DW (2019) Engineering dual-glycan responsive expression systems for tunable production of heterologous proteins in Bacteroides thetaiotaomicron. Sci Rep 9(1):17400. https://doi.org/10.1038/s41598-019-53726-w
Kahel-Raifer H, Jindou S, Bahari L, Nataf Y, Shoham Y, Bayer EA, Borovok I, Lamed R (2010) The unique set of putative membrane-associated anti-σ factors in Clostridium thermocellum suggests a novel extracellular carbohydrate-sensing mechanism involved in gene regulation. FEMS Microbiol Lett 308(1):84–93. https://doi.org/10.1111/j.1574-6968.2010.01997.x
Kaleta C, Schäuble S, Rinas U, Schuster S (2013) Metabolic costs of amino acid and protein production in Escherichia coli. Biotechnol J 8(9):1105–1114. https://doi.org/10.1002/biot.201200267
Kataeva IA, Yang SJ, Dam P, Poole FL, Yin Y, Zhou F, Chou WC, Xu Y, Goodwin L, Sims DR, Detter JC, Hauser LJ, Westpheling J, Adams MW (2009) Genome sequence of the anaerobic, thermophilic, and cellulolytic bacterium Anaerocellum thermophilum DSM 6725. J Bacteriol 191(11):3760–3761. https://doi.org/10.1128/JB.00256-09
Khan AMAM, Hauk VJ, Ibrahim M, Raffel TR, Blumer-Schuette SE (2020) Caldicellulosiruptor bescii adheres to polysaccharides via a type IV pilin-dependent mechanism. Appl Environ Microbiol 86(9). https://doi.org/10.1128/AEM.00200-20
Kim S-K, Chung D, Himmel ME, Bomble YJ, Westpheling J (2017a) Engineering the N-terminal end of CelA results in improved performance and growth of Caldicellulosiruptor bescii on crystalline cellulose. Biotechnol Bioeng 114(5):945–950. https://doi.org/10.1002/bit.26242
Kim SK, Chung D, Himmel ME, Bomble YJ, Westpheling J (2017b) In vivo synergistic activity of a CAZyme cassette from Acidothermus cellulolyticus significantly improves the cellulolytic activity of the C. bescii exoproteome. Biotechnol Bioeng 114(11):2474–2480. https://doi.org/10.1002/bit.26366
König H, Li L, Fröhlich J (2013) The cellulolytic system of the termite gut. Appl Microbiol Biotechnol 97(18):7943–7962. https://doi.org/10.1007/s00253-013-5119-z
Koonin EV, Wolf YI (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36(21):6688–6719. https://doi.org/10.1093/nar/gkn668
Korotkov KVS, M, Hol WGJ (2012) The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol 10(5):336–351. https://doi.org/10.1038/nrmicro2762
Kotrba PI M, Yukawa H (2001) Bacterial phosphotransferase system (PTS) in carbohydrate uptake and control of carbon metabolism. J Biosci Bioeng 92(6):502–517. https://doi.org/10.1016/S1389-1723(01)80308-X
Kurm V, van der Putten WH, Weidner S, Geisen S, Snoek BL, Bakx T, Hol WHG (2019) Competition and predation as possible causes of bacterial rarity. Environ Microbiol 21(4):1356–1368. https://doi.org/10.1111/1462-2920.14569
Lapébie P, Lombard V, Drula E, Terrapon N, Henrissat B (2019) Bacteroidetes use thousands of enzyme combinations to break down glycans. Nat Commun 10(1):2043. https://doi.org/10.1038/s41467-019-10068-5
Larsbrink J, Thompson AJ, Lundqvist M, Gardner JG, Davies GJ, Brumer H (2014) A complex gene locus enables xyloglucan utilization in the model saprophyte Cellvibrio japonicus. Mol Microbiol 94(2):418–433. https://doi.org/10.1111/mmi.12776
Lee LL, Crosby JR, Rubinstein GM, Laemthong T, Bing RG, Straub CT, Adams MWW, Kelly RM (2019a) The biology and biotechnology of the genus Caldicellulosiruptor: recent developments in ‘Caldi World.’ Extremophiles 24(1):1–15. https://doi.org/10.1007/s00792-019-01116-5
Lee LL, Hart WS, Lunin VV, Alahuhta M, Bomble YJ, Himmel ME, Blumer-Schuette SE, Adams MWW, Kelly RM (2019b) Comparative biochemical and structural analysis of novel cellulose binding proteins (Tāpirins) from extremely thermophilic. Appl Environ Microbiol 85(3). https://doi.org/10.1128/AEM.01983-18
Leigh JA, Dodsworth JA (2007) Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61:349–377. https://doi.org/10.1146/annurev.micro.61.080706.093409
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(1):41. https://doi.org/10.1186/1754-6834-6-41
Litchman E, Edwards KF, Klausmeier CA (2015) Microbial resource utilization traits and trade-offs: implications for community structure, functioning, and biogeochemical impacts at present and in the future. Front Microbiol 6:254. https://doi.org/10.3389/fmicb.2015.00254
Liu R, Liang L, Chen K, Ma J, Jiang M, Wei P, Ouyang P (2012) Fermentation of xylose to succinate by enhancement of ATP supply in metabolically engineered Escherichia coli. Appl Microbiol Biotechnol 94(4):959–968. https://doi.org/10.1007/s00253-012-3896-4
Lowe EC, BaslÈ A, Czjzek M, Firbank SJ, Bolam DN (2012) A scissor blade-like closing mechanism implicated in transmembrane signaling in a Bacteroides hybrid two-component system. Proc Natl Acad Sci U S A 109(19):7298–7303. https://doi.org/10.1073/pnas.1200479109
Lynch JB, Sonnenburg JL (2012) Prioritization of a plant polysaccharide over a mucus carbohydrate is enforced by a Bacteroides hybrid two-component system. Mol Microbiol 85(3):478–491. https://doi.org/10.1111/j.1365-2958.2012.08123.x
Mazzoli R, Olson DG, Lynd LR (2020) Construction of lactic acid overproducing Clostridium thermocellum through enhancement of lactate dehydrogenase expression. Enzyme Microb Technol 141:109645. https://doi.org/10.1016/j.enzmictec.2020.109645
McDonald R, Zhang F, Watts JEM, Schreier HJ (2015) Nitrogenase diversity and activity in the gastrointestinal tract of the wood-eating catfish Panaque nigrolineatus. ISME J 9(12):2712–2724. https://doi.org/10.1038/ismej.2015.65
McKee LS, La Rosa SL, Westereng B, Eijsink VG, Pope PB, Larsbrink J (2021) Polysaccharide degradation by the Bacteroidetes: mechanisms and nomenclature. Environ Microbiol Rep. https://doi.org/10.1111/1758-2229.12980
Miyashiro T, Klein W, Oehlert D, Cao X, Schwartzman J, Ruby EG (2011) The N-acetyl-D-glucosamine repressor NagC of Vibrio fischeri facilitates colonization of Euprymna scolopes. Mol Microbiol 82(4):894–903. https://doi.org/10.1111/j.1365-2958.2011.07858.x
Monge EC, Gardner JG (2021) Efficient chito-oligosaccharide utilization requires two TonB-dependent transporters and one hexosaminidase in Cellvibrio japonicus. Mol Microbiol. https://doi.org/10.1111/mmi.14717
Monge EC, Tuveng TR, Vaaje-Kolstad G, Eijsink VGH, Gardner JG (2018) Systems analysis of the glycoside hydrolase family 18 enzymes from. J Biol Chem 293(10):3849–3859. https://doi.org/10.1074/jbc.RA117.000849
Muir MW, L., Ferenci, T. (1985) Influence of transport energization on the growth yield of Escherichia coli. J Bacteriol 163(3):1237–1242. https://doi.org/10.1128/jb.163.3.1237-1242.1985
Muñoz-Gutiérrez I, Ortiz de Ora L, Rozman Grinberg I, Garty Y, Bayer EA, Shoham Y, Lamed R, Borovok I (2016) Decoding biomass-sensing regulons of Clostridium thermocellum alternative sigma-I factors in a heterologous Bacillus subtilis host system. PLoS ONE 11(1):e0146316. https://doi.org/10.1371/journal.pone.0146316
Nataf Y, Bahari L, Kahel-Raifer H, Borovok I, Lamed R, Bayer EA, Sonenshein AL, Shoham Y (2010) Clostridium thermocellum cellulosomal genes are regulated by extracytoplasmic polysaccharides via alternative sigma factors. Proc Natl Acad Sci U S A 107(43):18646–18651. https://doi.org/10.1073/pnas.1012175107
Ndeh D, Baslé A, Strahl H, Yates EA, McClurgg UL, Henrissat B, Terrapon N, Cartmell A (2020) Metabolism of multiple glycosaminoglycans by Bacteroides thetaiotaomicron is orchestrated by a versatile core genetic locus. Nat Commun 11(1):646. https://doi.org/10.1038/s41467-020-14509-4
Nelson CE, Attia MA, Rogowski A, Morland C, Brumer H, Gardner JG (2017a) Comprehensive functional characterization of the glycoside hydrolase family 3 enzymes from Cellvibrio japonicus reveals unique metabolic roles in biomass saccharification. Environ Microbiol 19(12):5025–5039. https://doi.org/10.1111/1462-2920.13959
Nelson CE, Gardner JG (2015) In-frame deletions allow functional characterization of complex cellulose degradation phenotypes in Cellvibrio japonicus. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00847-15
Nelson CE, Rogowski A, Morland C, Wilhide JA, Gilbert HJ, Gardner JG (2017b) Systems analysis in Cellvibrio japonicus resolves predicted redundancy of β-glucosidases and determines essential physiological functions. Mol Microbiol 104(2):294–305. https://doi.org/10.1111/mmi.13625
Novichkov PS, Kazakov AE, Ravcheev DA, Leyn SA, Kovaleva GY, Sutormin RA, Kazanov MD, Riehl W, Arkin AP, Dubchak I, Rodionov DA (2013) RegPrecise 3.0--a resource for genome-scale exploration of transcriptional regulation in bacteria. BMC Genomics 14:745. https://doi.org/10.1186/1471-2164-14-745
Ortiz de Ora L, Lamed R, Liu YJ, Xu J, Cui Q, Feng Y, Shoham Y, Bayer EA, Muñoz-Gutiérrez I (2018) Regulation of biomass degradation by alternative σ factors in cellulolytic clostridia. Sci Rep 8(1):11036. https://doi.org/10.1038/s41598-018-29245-5
Ortiz de Ora L, Muñoz-Gutiérrez I, Bayer EA, Shoham Y, Lamed R, Borovok I (2017) Revisiting the regulation of the primary scaffoldin gene in Clostridium thermocellum. Appl Environ Microbiol 83(8). https://doi.org/10.1128/AEM.03088-16
Osiro KOdC BR, Satomi R, Hamann PR, Silva JP, de Sousa MV, Quirino BF, Aquino EN, Felix CR, Murad AM, Noronha EF (2017) Characterization of Clostridium thermocellum (B8) secretome and purified cellulosomes for lignocellulosic biomass degradation. Enzyme Microb Technol 97:43–54. https://doi.org/10.1016/j.enzmictec.2016.11.002
Patel EH, Paul LV, Patrick S, Abratt VR (2008) Rhamnose catabolism in Bacteroides thetaiotaomicron is controlled by the positive transcriptional regulator RhaR. Res Microbiol 159(9–10):678–684. https://doi.org/10.1016/j.resmic.2008.09.002
Plumbridge JA (1991) Repression and induction of the nag regulon of Escherichia coli K-12: the roles of nagC and nagA in maintenance of the uninduced state. Mol Microbiol 5(8):2053–2062. https://doi.org/10.1111/j.1365-2958.1991.tb00828.x
Pollet RMM, LM, Koropatkin NM (2021) TonB-dependent transporters in the Bacteroidetes: unique domain structures and potential functions. Mol Microbiol 115(3):490–501. https://doi.org/10.1111/mmi.14683
Qi K, Chen C, Yan F, Feng Y, Bayer EA, Kosugi A, Cui Q, Liu YJ (2021) Coordinated β-glucosidase activity with the cellulosome is effective for enhanced lignocellulose saccharification. Bioresour Technol 337:125441. https://doi.org/10.1016/j.biortech.2021.125441
Rakoff-Nahoum S, Coyne MJ, Comstock LE (2013) An ecological network of polysaccharide utilization among human intestinal symbionts. Curr Biol 24(1):40–49. https://doi.org/10.1016/j.cub.2013.10.077
Raman B, McKeown CK, Rodriguez M Jr, Brown SD, Mielenz JR (2011) Transcriptomic analysis of Clostridium thermocellum ATCC 27405 cellulose fermentation. BMC Microbiol 11:134. https://doi.org/10.1186/1471-2180-11-134
Raman BPC, Hurst GB, Rodriguez M, McKeown CK, Lankford PK, Samatova NF, Mielenz JR (2009) Impact of pretreated Switchgrass and biomass carbohydrates on Clostridium thermocellum ATCC 27405 cellulosome composition: a quantitative proteomic analysis. PLoS One 4(4):e5271. https://doi.org/10.1371/journal.pone.0005271
Ravcheev DA, Godzik A, Osterman AL, Rodionov DA (2013) Polysaccharides utilization in human gut bacterium Bacteroides thetaiotaomicron: comparative genomics reconstruction of metabolic and regulatory networks. BMC Genomics 14:873. https://doi.org/10.1186/1471-2164-14-873
Ravcheev DA, Khoroshkin MS, Laikova ON, Tsoy OV, Sernova NV, Petrova SA, Rakhmaninova AB, Novichkov PS, Gelfand MS, Rodionov DA (2014) Comparative genomics and evolution of regulons of the LacI-family transcription factors. Front Microbiol 5:294. https://doi.org/10.3389/fmicb.2014.00294
Reitzer L (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57:155–176. https://doi.org/10.1146/annurev.micro.57.030502.090820
Riederer A, Takasuka TE, Makino S, Stevenson DM, Bukhman YV, Elsen NL, Fox BG (2011) Global gene expression patterns in Clostridium thermocellum as determined by microarray analysis of chemostat cultures on cellulose or cellobiose. Appl Environ Microbiol 77(4):1243–1253. https://doi.org/10.1128/AEM.02008-10
Rodionov DAR IA, Rodionov VA, Arzamasov AA, Zhang K, Rubinstein GM, Tanwee TNN, Bing RG, Crosby JR, Nookaew I, Basen M, Brown SD, Wilson CM, Klingeman DM, Poole FL, Zhang Y, Kelly RM, Adams MWW (2021) Transcriptional regulation of plant biomass degradation and carbohydrate utilization genes in the extreme thermophile Caldicellulosiruptor bescii. mSystems 6:e01345–20. https://doi.org/10.1128/mSystems.01345-20.
Rogers TE, Pudlo NA, Koropatkin NM, Bell JS, Moya Balasch M, Jasker K, Martens EC (2013) Dynamic responses of Bacteroides thetaiotaomicron during growth on glycan mixtures. Mol Microbiol 88(5):876–890. https://doi.org/10.1111/mmi.12228
Russell JBC, GM (1995) Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev 59(1):48–62
Rydzak TG,D, Stevenson DM, Sladek M, Klingeman DM, Holwerda EK, Amador-Noguez D, Brown SD, Guss AM (2017) Deletion of Type I glutamine synthetase deregulates nitrogen metabolism and increases ethanol production in Clostridium thermocellum. Metab Eng 41:182–191. https://doi.org/10.1016/j.ymben.2017.04.002
Sand A, Holwerda EK, Ruppertsberger NM, Maloney M, Olson DG, Nataf Y, Borovok I, Sonenshein AL, Bayer EA, Lamed R, Lynd LR, Shoham Y (2015) Three cellulosomal xylanase genes in Clostridium thermocellum are regulated by both vegetative SigA (σ(A)) and alternative SigI6 (σ(I6)) factors. FEBS Lett 589(20 Pt B):3133–40. https://doi.org/10.1016/j.febslet.2015.08.026
Sander K, Chung D, Hyatt D, Westpheling J, Klingeman DM, Rodriguez M, Engle NL, Tschaplinski TJ, Davison BH, Brown SD (2018) Rex in Caldicellulosiruptor bescii: Novel regulon members and its effect on the production of ethanol and overflow metabolites. Microbiologyopen 8(2):e00639. https://doi.org/10.1002/mbo3.639
Schreier HJ (1993) Biosynthesis of glutamine and glutamate and the assimilation of ammonia.281–298. https://doi.org/10.1128/9781555818388.ch20
Schreier HJ, Brown SW, Hirschi KD, Nomellini JF, Sonenshein AL (1989) Regulation of Bacillus subtilis glutamine synthetase gene expression by the product of the glnR gene. J Mol Biol 210(1):51–63. https://doi.org/10.1016/0022-2836(89)90290-8
Schwalm Iii ND, Townsend Ii GE, Groisman EA (2017) Prioritization of polysaccharide utilization and control of regulator activation in Bacteroides thetaiotaomicron. Mol Microbiol 104(1):32–45. https://doi.org/10.1111/mmi.13609
Schwalm ND, Groisman EA (2017) Navigating the gut buffet: control of polysaccharide utilization in Bacteroides spp. Trends Microbiol 25(12):1005–1015. https://doi.org/10.1016/j.tim.2017.06.009
Schwalm ND, Townsend GE, Groisman EA (2016) Multiple signals govern utilization of a polysaccharide in the gut bacterium Bacteroides thetaiotaomicron. mBio 7(5). https://doi.org/10.1128/mBio.01342-16
Sebestyén Z, Jakab E, Domán A, Bokrossy P, Bertóti I, Madarász J, László K (2020) Thermal degradation of crab shell biomass, a nitrogen-containing carbon precursor. J Therm Anal Calorim 142(1):301–308. https://doi.org/10.1007/s10973-020-09438-9
Shilev S, Naydenov M, Vancheva V, Aladjadjiyan A Composting of food and agricultural wastes. In: Oreopoulou V, Russ W (eds) Utilization of By-Products and Treatment of Waste in the Food Industry, Boston, MA, 2007// 2007. Springer US, p 283–301
Shulami S, Zaide G, Zolotnitsky G, Langut Y, Feld G, Sonenshein AL, Shoham Y (2006) A two-component system regulates the expression of an ABC transporter for xylo-oligosaccharides in Geobacillus stearothermophilus. Appl Environ Microbiol 73(3):874–884. https://doi.org/10.1128/AEM.02367-06
Sivashankari PR, Prabaharan M (2017) 5 - Deacetylation modification techniques of chitin and chitosan. In: Jennings JA, Bumgardner JD (eds) Chitosan Based Biomaterials, vol 1. Woodhead Publishing, pp 117–133
Sonenshein AL (2005) CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol 8(2):203–207. https://doi.org/10.1016/j.mib.2005.01.001
Stevenson DM, Weimer PJ (2005) Expression of 17 genes in Clostridium thermocellum ATCC 27405 during fermentation of cellulose or cellobiose in continuous culture. Appl Environ Microbiol 71(8):4672–4678. https://doi.org/10.1128/AEM.71.8.4672-4678.2005
Stouthamer AH (1973) A theoretical study on the amount of ATP required for synthesis of microbial cell material. Antonie Van Leeuwenhoek 39(3):545–565. https://doi.org/10.1007/BF02578899
Straub CT, Bing RG, Wang JP, Chiang VL, Adams MWW, Kelly RM (2020) Use of the lignocellulose-degrading bacterium. Biotechnol Biofuels 13:43. https://doi.org/10.1186/s13068-020-01675-2
Stubbendieck RM, Straight PD (2016) Multifaceted Interfaces of bacterial competition. J Bacteriol 198(16):2145–2155. https://doi.org/10.1128/JB.00275-16
Su X, Mackie RI, Cann IK (2012) Biochemical and mutational analyses of a multidomain cellulase/mannanase from Caldicellulosiruptor bescii. Appl Environ Microbiol 78(7):2230–2240. https://doi.org/10.1128/AEM.06814-11
Tang K, Jiao N, Liu K, Zhang Y, Li S (2012) Distribution and functions of TonB-dependent transporters in marine bacteria and environments: implications for dissolved organic matter utilization. PLoS ONE 7(7):e41204. https://doi.org/10.1371/journal.pone.0041204
Terrapon N, Lombard V, Gilbert HJ, Henrissat B (2014) Automatic prediction of polysaccharide utilization loci in Bacteroidetes species. Bioinformatics 31(5):647–655. https://doi.org/10.1093/bioinformatics/btu716
Tian L, Conway PM, Cervenka ND, Cui J, Maloney M, Olson DG, Lynd LR (2019) Metabolic engineering of Clostridium thermocellum for n-butanol production from cellulose. Biotechnol Biofuels 12(1):186. https://doi.org/10.1186/s13068-019-1524-6
Townsend GE, Han W, Schwalm ND, Hong X, Bencivenga-Barry NA, Goodman AL, Groisman EA (2020) A master regulator of Bacteroides thetaiotaomicron gut colonization controls carbohydrate utilization and an alternative protein synthesis factor. mBio 11(1). https://doi.org/10.1128/mBio.03221-19
Tripathi SA, Olson DG, Argyros DA, Miller BB, Barrett TF, Murphy DM, McCool JD, Warner AK, Rajgarhia VB, Lynd LR, Hogsett DA, Caiazza NC (2010) Development of pyrF-based genetic system for targeted gene deletion in Clostridium thermocellum and creation of a pta mutant. Appl Environ Microbiol 76(19):6591–6599. https://doi.org/10.1128/AEM.01484-10
Ueda KI, S, Itami T, Asai T (1952) Studies on the aerobic mesophilic cellulose-decomposing bacteria. Part 5-2. Taxonomical study on genus Pseudomonas. J Agric Chem Soc 26:35–41
Valguarnera E, Scott NE, Azimzadeh P, Feldman MF (2018) Surface exposure and packing of lipoproteins into outer membrane vesicles are coupled processes in. mSphere 3(6). https://doi.org/10.1128/mSphere.00559-18
van Heeswijk WC, Molenaar D, Hoving S, Westerhoff HV (2009) The pivotal regulator GlnB of Escherichia coli is engaged in subtle and context-dependent control. FEBS J 276(12):3324–3340. https://doi.org/10.1111/j.1742-4658.2009.07058.x
Watts JEM, McDonald R, Daniel R, Schreier HJ (2013) Examination of a culturable microbial population from the gastrointestinal tract of the wood-eating loricariid catfish Panaque nigrolineatus. Diversity 5(3). https://doi.org/10.3390/d5030641
Watts JEM, McDonald RC, Schreier HJ (2021) Wood degradation by Panaque nigrolineatus, a neotropical catfish: diversity and activity of gastrointestinal tract lignocellulolytic and nitrogen fixing communities Advances in Botanical Research. Academic Press
Wei Z, Chen C, Liu YJ, Dong S, Li J, Qi K, Liu S, Ding X, Ortiz de Ora L, Muñoz-Gutiérrez I, Li Y, Yao H, Lamed R, Bayer EA, Cui Q, Feng Y (2019) Alternative σI/anti-σI factors represent a unique form of bacterial σ/anti-σ complex. Nucleic Acids Res 47(11):5988–5997. https://doi.org/10.1093/nar/gkz355
Wiegel JD M (1984) Clostridium thermocellum: adhesion and sporulation while adhered to cellulose and hemicellulose. Appl Microbiol Biotechnol 20:59-65. https://doi.org/10.1007/BF00254647
Wilson CM, Klingeman DM, Schlachter C, Syed MH, Wu CW, Guss AM, Brown SD (2017) LacI transcriptional regulatory networks in Clostridium thermocellum DSM1313. Appl Environ Microbiol 83(5). https://doi.org/10.1128/AEM.02751-16
Wray LV, Zalieckas JM, Fisher SH (2000) Purification and in vitro activities of the Bacillus subtilis TnrA transcription factor. J Mol Biol 300(1):29–40. https://doi.org/10.1006/jmbi.2000.3846
Xu J, Bjursell MK, Himrod J, Deng S, Carmichael LK, Chiang HC, Hooper LV, Gordon JI (2003) A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299(5615):2074–2076. https://doi.org/10.1126/science.1080029
Yang SJ, Kataeva I, Wiegel J, Yin Y, Dam P, Xu Y, Westpheling J, Adams MWW (2009) Classification of Anaerocellum thermophilum strain DSM 6725 as Caldicellulosiruptor bescii sp. nov. Int J Syst Evol Microbiol 60(Pt 9):2011–2015. https://doi.org/10.1099/ijs.0.017731-0
Yang Y, Zhang L, Huang H, Yang C, Yang S, Gu Y, Jiang W (2017) A flexible binding site architecture provides new insights into CcpA global regulation in Gram-positive bacteria. mBio 8(1). https://doi.org/10.1128/mBio.02004-16
Yokoyama H, Yamashita T, Morioka R, Ohmori H (2014) Extracellular secretion of noncatalytic plant cell wall-binding proteins by the cellulolytic thermophile Caldicellulosiruptor bescii. J Bacteriol 196(21):3784–3792. https://doi.org/10.1128/JB.01897-14
Zhang FL J, Liu H, Liang Q, Qi Q (2016) ATP-based ratio regulation of glucose and xylose improved succinate production. PLoS One 11(6):e0157775. https://doi.org/10.1371/journal.pone.0157775
Zhang J, Liu S, Li R, Hong W, Xiao Y, Feng Y, Cui Q, Liu YJ (2017) Efficient whole-cell-catalyzing cellulose saccharification using engineered. Biotechnol Biofuels 10:124. https://doi.org/10.1186/s13068-017-0796-y
Zurawski JV, Conway JM, Lee LL, Simpson HJ, Izquierdo JA, Blumer-Schuette S, Nookaew I, Adams MW, Kelly RM (2015) Comparative analysis of extremely thermophilic Caldicellulosiruptor species reveals common and unique cellular strategies for plant biomass utilization. Appl Environ Microbiol 81(20):7159–7170. https://doi.org/10.1128/AEM.01622-15
Funding
Work in the lab of JGG was supported by the US Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Number DE-SC0014183. Work in the lab of HJS was supported, in part, by a grant from the National Science Foundation under Award Number 0801830.
Author information
Authors and Affiliations
Contributions
Both JGG and HJS contributed to the writing and editing of this review.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gardner, J.G., Schreier, H.J. Unifying themes and distinct features of carbon and nitrogen assimilation by polysaccharide-degrading bacteria: a summary of four model systems. Appl Microbiol Biotechnol 105, 8109–8127 (2021). https://doi.org/10.1007/s00253-021-11614-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-021-11614-2