Functional Diversity of Carbohydrate-Active Enzymes Enabling a Bacterium to Ferment Plant Biomass

English version České info

Plant-fermenting bacteria are important for the global carbon cycle, human nutrition, and industrial production of renewable fuels and commodities from cellulosic biomass. Plants are primarily composed of heterogeneous polysaccharides, requiring plant-degrading microbes to encode many carbohydrate-active enzymes (CAZymes) to cleave different sugar linkages. Here we develop a broadly applicable method to study how microbes catabolize plant biomass by determining the combination of CAZymes that depolymerize each polysaccharide into sugars, how the cell alters global mRNA expression, and the efficiency with which each polysaccharide is metabolized. We apply this method to investigate how Clostridium phytofermentans, a bacterium encoding 171 CAZymes, ferments polysaccharides. We assimilate our results into a genetic model of how this bacterium metabolizes plant biomass and discuss how these results further our understanding of microbial plant fermentation.

Vyšlo v časopise: Functional Diversity of Carbohydrate-Active Enzymes Enabling a Bacterium to Ferment Plant Biomass. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004773
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004773

Souhrn

Zdroje

1. ShekharC (2011) Future fuel: could biomass be the new petroleum? Chem Biol 18: 1199–1200 doi:10.1016/j.chembiol.2011.10.010

2. SchwarzWH (2001) The cellulosome and cellulose degradation by anaerobic bacteria. Appl Microbiol Biotechnol 56: 634–649 doi:10.1007/s002530100710

3. EdwardsJL, SmithDL, ConnollyJ, McDonaldJE, CoxMJ, et al. (2010) Identification of carbohydrate metabolism genes in the metagenome of a marine biofilm community shown to be dominated by gammaproteobacteria and bacteroidetes. Genes 1: 371–384 doi:10.3390/genes1030371

4. McNeilNI (1984) The contribution of the large intestine to energy supplies in man. Am J Clin Nutr 39: 338–342.

5. PaulyM, KeegstraK (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J Cell Mol Biol 54: 559–568 doi:10.1111/j.1365-313X.2008.03463.x

6. El KaoutariA, ArmougomF, GordonJI, RaoultD, HenrissatB (2013) The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol 11: 497–504 doi:10.1038/nrmicro3050

7. DeutschmannR, DekkerRFH (2012) From plant biomass to bio-based chemicals: latest developments in xylan research. Biotechnol Adv 30: 1627–1640 doi:10.1016/j.biotechadv.2012.07.001

8. BauerWD, TalmadgeKW, KeegstraK, AlbersheimP (1973) The Structure of Plant Cell Walls: II. The Hemicellulose of the Walls of Suspension-cultured Sycamore Cells. Plant Physiol 51: 174–187 doi:http://dx.doi.org/10.1104/pp.51.1.174

9. BurkeD, KaufmanP, McNeilM, AlbersheimP (1974) The Structure of Plant Cell Walls: VI. A Survey of the Walls of Suspension-cultured Monocots. Plant Physiol 54: 109–115 doi:http://dx.doi.org/10.1104/pp.54.1.109

10. CapekP, AlföldiJ, LiskováD (2002) An acetylated galactoglucomannan from Picea abies L. Karst. Carbohydr Res 337: 1033–1037 doi:10.1016/S0008-6215(02)00090-3

11. BuckeridgeMS (2010) Seed cell wall storage polysaccharides: models to understand cell wall biosynthesis and degradation. Plant Physiol 154: 1017–1023 doi:10.1104/pp.110.158642

12. CaffallKH, MohnenD (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344: 1879–1900 doi:10.1016/j.carres.2009.05.021

13. RidleyBL, O'NeillMA, MohnenD (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57: 929–967 doi:10.1016/S0031-9422(01)00113-3

14. MohnenD (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11: 266–277 doi:10.1016/j.pbi.2008.03.006

15. LombardV, Golaconda RamuluH, DrulaE, CoutinhoPM, HenrissatB (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42: D490–495 doi:10.1093/nar/gkt1178

16. LyndLR, WeimerPJ, van ZylWH, PretoriusIS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev MMBR 66: 506–577 table of contents. doi:10.1128/MMBR.66.3.506-577.2002

17. Tolonen AC, Petit E, Blanchard JL, Warnick T, Leschine SB (2013) Technologies to Study Plant Biomass Fermentation Using the Model Bacterium Clostridium phytofermentans. In: J. Sun, S.Y. Ding, J.D. Peterson (Eds.), Biological conversion of biomass for fuels and chemicals, Royal Society of Chemistry, Cambridge, pp. 114–139. doi:10.1039/9781849734738-00114

18. WarnickTA, MethéBA, LeschineSB (2002) Clostridium phytofermentans sp. nov., a cellulolytic mesophile from forest soil. Int J Syst Evol Microbiol 52: 1155–1160 doi:10.1099/ijs.0.02125-0

19. HatfieldRD, WeimerPJ (1995) Degradation characteristics of isolated and in situ cell wall lucerne pectic polysaccharides by mixed ruminal microbes. J Sci Food Agric 69: 185–196 doi:10.1002/jsfa.2740690208

20. MartensEC, LoweEC, ChiangH, PudloNA, WuM, et al. (2011) Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts. PLoS Biol 9: e1001221 doi:10.1371/journal.pbio.1001221

21. MuirM, WilliamsL, FerenciT (1985) Influence of transport energization on the growth yield of Escherichia coli. J Bacteriol 163: 1237–1242.

22. ZhangY-HP, LyndLR (2005) Cellulose utilization by Clostridium thermocellum: bioenergetics and hydrolysis product assimilation. Proc Natl Acad Sci U S A 102: 7321–7325 doi:10.1073/pnas.0408734102

23. NihiraT, NakaiH, ChikuK, KitaokaM (2012) Discovery of nigerose phosphorylase from Clostridium phytofermentans. Appl Microbiol Biotechnol 93: 1513–1522 doi:10.1007/s00253-011-3515-9

24. NakajimaM, NishimotoM, KitaokaM (2009) Characterization of three beta-galactoside phosphorylases from Clostridium phytofermentans: discovery of d-galactosyl-beta1->4-l-rhamnose phosphorylase. J Biol Chem 284: 19220–19227 doi:10.1074/jbc.M109.007666

25. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106 doi:10.1186/gb-2010-11-10-r106

26. TolonenAC, CerisyT, El-SayyedH, BoutardM, SalanoubatM, et al. (2014) Fungal lysis by a soil bacterium fermenting cellulose. Environ Microbiol doi:10.1111/1462-2920.12495

27. TolonenAC, ChilakaAC, ChurchGM (2009) Targeted gene inactivation in Clostridium phytofermentans shows that cellulose degradation requires the family 9 hydrolase Cphy3367. Mol Microbiol 74: 1300–1313 doi:10.1111/j.1365-2958.2009.06890.x

28. ZhangX-Z, SathitsuksanohN, ZhangY-HP (2010) Glycoside hydrolase family 9 processive endoglucanase from Clostridium phytofermentans: heterologous expression, characterization, and synergy with family 48 cellobiohydrolase. Bioresour Technol 101: 5534–5538 doi:10.1016/j.biortech.2010.01.152

29. ZhangX-Z, ZhangZ, ZhuZ, SathitsuksanohN, YangY, et al. (2010) The noncellulosomal family 48 cellobiohydrolase from Clostridium phytofermentans ISDg: heterologous expression, characterization, and processivity. Appl Microbiol Biotechnol 86: 525–533 doi:10.1007/s00253-009-2231-1

30. KnoxJP (2008) Revealing the structural and functional diversity of plant cell walls. Curr Opin Plant Biol 11: 308–313 doi:10.1016/j.pbi.2008.03.001

31. AbbottDW, HrynuikS, BorastonAB (2007) Identification and characterization of a novel periplasmic polygalacturonic acid binding protein from Yersinia enterolitica. J Mol Biol 367: 1023–1033 doi:10.1016/j.jmb.2007.01.030

32. AspeborgH, CoutinhoPM, WangY, BrumerH, HenrissatB (2012) Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 12: 186 doi:10.1186/1471-2148-12-186

33. LiaoH, ZhangX-Z, RollinJA, ZhangY-HP (2011) A minimal set of bacterial cellulases for consolidated bioprocessing of lignocellulose. Biotechnol J 6: 1409–1418 doi:10.1002/biot.201100157

34. BenzJP, ChauBH, ZhengD, BauerS, GlassNL, et al. (2014) A comparative systems analysis of polysaccharide-elicited responses in Neurospora crassa reveals carbon source-specific cellular adaptations. Mol Microbiol 91: 275–299 doi:10.1111/mmi.12459

35. NöllingJ, BretonG, OmelchenkoMV, MakarovaKS, ZengQ, et al. (2001) Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J Bacteriol 183: 4823–4838 doi:10.1128/JB.183.16.4823-4838.2001

36. Al MakishahNH, MitchellWJ (2013) Dual substrate specificity of an N-acetylglucosamine phosphotransferase system in Clostridium beijerinckii. Appl Environ Microbiol 79: 6712–6718 doi:10.1128/AEM.01866-13

37. ServinskyMD, KielJT, DupuyNF, SundCJ (2010) Transcriptional analysis of differential carbohydrate utilization by Clostridium acetobutylicum. Microbiol Read Engl 156: 3478–3491 doi:10.1099/mic.0.037085-0

38. ChenM, ChenL, ZouY, XueM, LiangM, et al. (2011) Wide sugar substrate specificity of galactokinase from Streptococcus pneumoniae TIGR4. Carbohydr Res 346: 2421–2425 doi:10.1016/j.carres.2011.08.014

39. ServinskyMD, GermaneKL, LiuS, KielJT, ClarkAM, et al. (2012) Arabinose is metabolized via a phosphoketolase pathway in Clostridium acetobutylicum ATCC 824. J Ind Microbiol Biotechnol 39: 1859–1867 doi:10.1007/s10295-012-1186-x

40. NgTK, Ben-BassatA, ZeikusJG (1981) Ethanol Production by Thermophilic Bacteria: Fermentation of Cellulosic Substrates by Cocultures of Clostridium thermocellum and Clostridium thermohydrosulfuricum. Appl Environ Microbiol 41: 1337–1343.

41. XuC, HuangR, TengL, WangD, HemmeCL, et al. (2013) Structure and regulation of the cellulose degradome in Clostridium cellulolyticum. Biotechnol Biofuels 6: 73 doi:10.1186/1754-6834-6-73

42. TolonenAC, HaasW (2014) Quantitative Proteomics Using Reductive Dimethylation for Stable Isotope Labeling. J Vis Exp (89) e51416 doi:10.3791/51416

43. JohnsonEA, MadiaA, DemainAL (1981) Chemically Defined Minimal Medium for Growth of the Anaerobic Cellulolytic Thermophile Clostridium thermocellum. Appl Environ Microbiol 41: 1060–1062.

44. HongJ, YeX, WangY, ZhangY-HP (2008) Bioseparation of recombinant cellulose-binding module-proteins by affinity adsorption on an ultra-high-capacity cellulosic adsorbent. Anal Chim Acta 621: 193–199 doi:10.1016/j.aca.2008.05.041

45. TolonenAC, HaasW, ChilakaAC, AachJ, GygiSP, et al. (2011) Proteome-wide systems analysis of a cellulosic biofuel-producing microbe. Mol Syst Biol 7: 461 doi:10.1038/msb.2010.116

46. DeAngelisMM, WangDG, HawkinsTL (1995) Solid-phase reversible immobilization for the isolation of PCR products. Nucleic Acids Res 23: 4742–4743 doi:10.1093/nar/23.22.4742

47. RohlandN, ReichD (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 22: 939–946 doi:10.1101/gr.128124.111

48. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25 doi:10.1186/gb-2009-10-3-r25

49. HabeggerL, SbonerA, GianoulisTA, RozowskyJ, AgarwalA, et al. (2011) RSEQtools: a modular framework to analyze RNA-Seq data using compact, anonymized data summaries. Bioinforma Oxf Engl 27: 281–283 doi:10.1093/bioinformatics/btq643

50. MandlikA, LivnyJ, RobinsWP, RitchieJM, MekalanosJJ, et al. (2011) RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe 10: 165–174 doi:10.1016/j.chom.2011.07.007

51. AslanidisC, de JongPJ (1990) Ligation-independent cloning of PCR products (LIC-PCR). Nucleic Acids Res 18: 6069–6074 http://dx.doi.org/10.1093/nar/18.20.6069.

52. PetersenTN, BrunakS, von HeijneG, NielsenH (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785–786 doi:10.1038/nmeth.1701

53. MillerGL (1959) Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Anal Chem 31: 426–428 doi:10.1021/ac60147a030

54. WatanabeT, ItoY, YamadaT, HashimotoM, SekineS, et al. (1994) The roles of the C-terminal domain and type III domains of chitinase A1 from Bacillus circulans WL-12 in chitin degradation. J Bacteriol 176: 4465–4472.

55. PetitE, LaToufWG, CoppiMV, WarnickTA, CurrieD, et al. (2013) Involvement of a bacterial microcompartment in the metabolism of fucose and rhamnose by Clostridium phytofermentans. PloS One 8: e54337 doi:10.1371/journal.pone.0054337

56. ZablackisE, HuangJ, MüllerB, DarvillAG, AlbersheimP (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107: 1129–1138 doi:http://dx.doi.org/10.1104/pp.107.4.1129

57. PrasadS, SinghA, JoshiHC (2007) Ethanol as an alternative fuel from agricultural, industrial and urban residues. Resour Conserv Recycl 50: 1–39 doi:10.1016/j.resconrec.2006.05.007

58. ChowPS, LandhäusserSM (2004) A method for routine measurements of total sugar and starch content in woody plant tissues. Tree Physiol 24: 1129–1136 doi:10.1093/treephys/24.10.1129

59. SchellerHV, UlvskovP (2010) Hemicelluloses. Annu Rev Plant Biol 61: 263–289 doi:10.1146/annurev-arplant-042809-112315

60. DahalP, NevinsDJ, BradfordKJ (1997) Relationship of Endo-[beta]-D-Mannanase Activity and Cell Wall Hydrolysis in Tomato Endosperm to Germination Rates. Plant Physiol 113: 1243–1252 doi:http://dx.doi.org/10.1104/pp.113.4.1243

61. PettolinoFA, WalshC, FincherGB, BacicA (2012) Determining the polysaccharide composition of plant cell walls. Nat Protoc 7: 1590–1607 doi:10.1038/nprot.2012.081

62. Oxenboll SørensenS, PaulyM, BushM, SkjøtM, McCannMC, et al. (2000) Pectin engineering: modification of potato pectin by in vivo expression of an endo-1,4-beta-D-galactanase. Proc Natl Acad Sci U S A 97: 7639–7644 doi:10.1073/pnas.130568297

63. MooreJP, Nguema-OnaE, ChevalierL, LindseyGG, BrandtWF, et al. (2006) Response of the leaf cell wall to desiccation in the resurrection plant Myrothamnus flabellifolius. Plant Physiol 141: 651–662 doi:10.1104/pp.106.077701