A polysaccharide utilization locus from an uncultured Bacteroidetes phylotype suggests ecological adaptation and substrate versatility

Applied and Environmental Microbiology

Volumn 81, Issue 1, 2015, Pages 187-195

  Mackenzie, A K ^a   Naas, A E ^a   Kracun, S K ^b   Schuckel J ^b   Fangel, J U ^b   Agger, J W ^a   Willats, W G T ^b   Eijsink, V G H ^a   Pope, Phillip B ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; CELLULOSE; CHEMICAL DETECTION; CHROMATOGRAPHY; ENZYMES; HYDROLASES; LIPOPROTEINS; MACHINERY; PLANTS (BOTANY); POLYSACCHARIDES; SUGARS;

ACTIVITY ENHANCEMENT; ANION EXCHANGE CHROMATOGRAPHY; BINDING SPECIFICITIES; CHROMOGENIC SUBSTRATE; ELECTROCHEMICAL DETECTION; GENE ORGANIZATION; GLYCOSIDE HYDROLASES; METAGENOMIC ANALYSIS;

SUBSTRATES;

ABUNDANCE; BIOMASS; CELLULOSE; CHROMOSOME; DEER; ENZYME ACTIVITY; POLYSACCHARIDE; SUBSTRATE; SYNERGISM;

RANGIFER TARANDUS; UNCULTURED BACTERIUM; UNCULTURED BACTEROIDETES BACTERIUM;

GLYCOSIDASE; POLYSACCHARIDE; PROTEIN BINDING;

ADAPTATION; ANIMAL; BACTEROIDETES; DNA SEQUENCE; ELECTROCHEMICAL ANALYSIS; ENZYME SPECIFICITY; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; METAGENOMICS; MICROBIOLOGY; MOLECULAR GENETICS; REINDEER; RUMINANT STOMACH; SVALBARD AND JAN MAYEN;

ADAPTATION, BIOLOGICAL; ANIMALS; BACTEROIDETES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTROCHEMICAL TECHNIQUES; GLYCOSIDE HYDROLASES; METABOLIC NETWORKS AND PATHWAYS; METAGENOMICS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTEIN BINDING; REINDEER; RUMEN; SEQUENCE ANALYSIS, DNA; SUBSTRATE SPECIFICITY; SVALBARD;

EID: 84917710956     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02858-14     Document Type: Article

References (37)

1. Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, McNulty NP, Abbott DW, Henrissat B, Gilbert HJ, Bolam DN, Gordon JI. 2011. Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 9:e1001221. http://dx.doi.org/10.1371/journal.pbio.1001221.
2. Martens EC, Koropatkin NM, Smith TJ, Gordon JI. 2009. Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Suslike paradigm. J Biol Chem 284:24673-24677. http://dx.doi.org/10.1074/jbc.R109.022848.
3. Koropatkin NM, Cameron EA, Martens EC. 2012. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10:323-335. http://dx.doi.org/10.1038/nrmicro2746.
4. Dodd D, Moon YH, Swaminathan K, Mackie RI, Cann IK. 2010. Transcriptomic analyses of xylan degradation by Prevotella bryantii and insights into energy acquisition by xylanolytic Bacteroidetes. J Biol Chem 285:30261-30273. http://dx.doi.org/10.1074/jbc.M110.141788.
5. Schauer K, Rodionov DA, de Reuse H. 2008. New substrates for TonBdependent transport: do we only see the 'tip of the iceberg'? Trends Biochem Sci 33:330-338. http://dx.doi.org/10.1016/j.tibs.2008.04.012.
6. Ferguson AD, Deisenhofer J. 2002. TonB-dependent receptors-structural perspectives. Biochim Biophys Acta 1565:318-332. http://dx.doi.org/10.1016/S0005-2736(02)00578-3.
7. Koropatkin NM, Martens EC, Gordon JI, Smith TJ. 2008. Starch catabolism by a prominent human gut symbiont is directed by the recognition of amylose helices. Structure 16:1105-1115. http://dx.doi.org/10.1016/j.str.2008.03.017.
8. Hehemann JH, Kelly AG, Pudlo NA, Martens EC, Boraston AB. 2012. Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci U S A 109:19786-19791. http://dx.doi.org/10.1073/pnas.1211002109.
9. Sonnenburg ED, Zheng H, Joglekar P, Higginbottom SK, Firbank SJ, Bolam DN, Sonnenburg JL. 2010. Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations. Cell 141:1241-1252. http://dx.doi.org/10.1016/j.cell.2010.05.005.
10. Larsbrink J, Rogers TE, Hemsworth GR, McKee LS, Tauzin AS, Spadiut O, Klinter S, Pudlo NA, Urs K, Koropatkin NM, Creagh AL, Haynes CA, Kelly AG, Cederholm SN, Davies GJ, Martens EC, Brumer H. 2014. A discrete genetic locus confers xyloglucan metabolism in select human gut Bacteroidetes. Nature 506:498-502. http://dx.doi.org/10.1038/nature12907.
11. Edwards JE, McEwan NR, Travis AJ, Wallace RJ. 2004. 16S rDNA library-based analysis of ruminal bacterial diversity. Antonie Van Leeuwenhoek 86:263-281. http://dx.doi.org/10.1023/B:ANTO.0000047942.69033.24.
12. Pope PB, Mackenzie AK, Gregor I, Smith W, Sundset MA, McHardy AC, Morrison M, Eijsink VGH. 2012. Metagenomics of the Svalbard reindeer rumen microbiome reveals abundance of polysaccharide utilization loci. PLoS One 7:e38571. http://dx.doi.org/10.1371/journal.pone.0038571.
13. Pope PB, Denman SE, Jones M, Tringe SG, Barry K, Malfatti SA, McHardy AC, Cheng J-F, Hugenholtz P, McSweeney CS, Morrison M. 2010. Adaptation to herbivory by the Tammar wallaby includes bacterial and glycoside hydrolase profiles different to other herbivores. Proc Natl Acad Sci U S A 107:14793-14798. http://dx.doi.org/10.1073/pnas.1005297107.
14. Rosewarne CP, Pope PB, Cheung JL, Morrison M. 2014. Analysis of the bovine rumen microbiome reveals a diversity of Sus-like polysaccharide utilization loci from the bacterial phylum Bacteroidetes. J Ind Microbiol Biotechnol 41:601-606. http://dx.doi.org/10.1007/s10295-013-1395-y.
15. 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. http://dx.doi.org/10.1126/science.1200387.
16. Patil KR, Haider P, Pope PB, Turnbaugh PJ, Morrison M, Scheffer T, McHardy AC. 2011. Taxonomic metagenome sequence assignment with structured output models. Nat Methods 8:191-192. http://dx.doi.org/10.1038/nmeth0311-191.
17. Mackenzie AK, Pope PB, Pedersen HL, Gupta R, Morrison M, Willats WG, Eijsink VGH. 2012. Two SusD-like proteins encoded within a polysaccharide utilization locus of an uncultured ruminant Bacteroidetes phylotype bind strongly to cellulose. Appl Environ Microbiol 78:5935-5937. http://dx.doi.org/10.1128/AEM.01164-12.
18. Moller I, Sørensen I, Bernal AJ, Blaukopf C, Lee K, Øbro J, Pettolino F, Roberts A, Mikkelsen JD, Knox JP, Bacic A, Willats WG. 2007. Highthroughput mapping of cell-wall polymers within and between plants using novel microarrays. Plant J 50:1118-1128. http://dx.doi.org/10.1111/j.1365-313X.2007.03114.x.
19. Moller IE, Pettolino FA, Hart C, Lampugnani ER, Willats WG, Bacic A. 2012. Glycan profiling of plant cell wall polymers using microarrays. J Vis Exp 70:e4238. http://dx.doi.org/10.3791/4238.
20. Sørmo W, Haga ØE Gaare E, Langvatn R, Mathiesen SD. 1999. Forage chemistry and fermentation chambers in Svalbard reindeer (Rangifer tarandus platyrhynchus). J Zool Lond 247:247-256. http://dx.doi.org/10.1111/j.1469-7998.1999.tb00988.x.
21. Orpin CG, Mathiesen SD, Greenwood Y, Blix AS. 1985. Seasonal changes in the ruminal microflora of the high-arctic Svalbard reindeer (Rangifer tarandus platyrhynchus). Appl Environ Microbiol 50:144-151.
22. Aslanidis C, de Jong PJ. 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.
23. Ten LN, Im W, Kim MK, Kang MS, Lee ST. 2004. Development of a plate technique for screening of polysaccharide-degrading microorganisms by using a mixture of insoluble chromogenic substrates. J Microbiol Methods 56:375-382. http://dx.doi.org/10.1016/j.mimet.2003.11.008.
24. Wood TM. 1988. Preparation of crystalline, amorphous, and dyed cellulase substrates. Methods Enzymol 160:19-25. http://dx.doi.org/10.1016/0076-6879(88)60103-0.
25. Miller GL. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426-428. http://dx.doi.org/10.1021/ac60147a030.
26. Vogel J. 2008. Unique aspects of the grass cell wall. Curr Opin Plant Biol 11:301-307. http://dx.doi.org/10.1016/j.pbi.2008.03.002.
27. Popper ZA, Fry SC. 2003. Primary cell wall composition of bryophytes and charophytes. Ann Bot 91:1-12. http://dx.doi.org/10.1093/aob/mcg013.
28. Aspeborg H, Coutinho PM, Wang Y, Brumer H, Henrissat B. 2012. Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5). BMC Evol Biol 12:186. http://dx.doi.org/10.1186/1471-2148-12-186.
29. Gardner RG, Wells JE, Fields MW, Wilson DB, Russell JB. 1997. A Prevotella ruminicola B(1)4 operon encoding extracellular polysaccharide hydrolases. Curr Microbiol 35:274-277. http://dx.doi.org/10.1007/s002849900253.
30. Qi M, Jun HS, Forsberg CW. 2008. Cel9D, an atypical 1,4-beta-D-glucan glucohydrolase from Fibrobacter succinogenes: characteristics, catalytic residues, and synergistic interactions with other cellulases. J Bacteriol 190: 1976-1984. http://dx.doi.org/10.1128/JB.01667-07.
31. Hazlewood GP, Davidson K, Laurie JI, Romaniec MP, Gilbert HJ. 1990. Cloning and sequencing of the celA gene encoding endoglucanase A of Butyrivibrio fibrisolvens strain A46. J Gen Microbiol 136:2089-2097. http://dx.doi.org/10.1099/00221287-136-10-2089.
32. Kirby J, Martin JC, Daniel AS, Flint HJ. 1997. Dockerin-like sequences in cellulases and xylanases from the rumen cellulolytic bacterium Ruminococcus flavefaciens. FEMS Microbiol Lett 149:213-219. http://dx.doi.org/10.1016/S0378-1097(97)00078-5.
33. Wang L, Hatem A, Catalyurek UV, Morrison M, Yu Z. 2013. Metagenomic insights into the carbohydrate-active enzymes carried by the microorganisms adhering to solid digesta in the rumen of cows. PLoS One 8:e78507. http://dx.doi.org/10.1371/journal.pone.0078507.
34. Naas AE, Mackenzie AK, Mravec J, Schückel J, Willats WG, Eijsink VG, Pope PB. 2014. Do rumen Bacteroidetes utilize an alternative mechanism for cellulose degradation? mBio 5(4):e01401-14. http://dx.doi.org/10.1128/mBio.01401-14.
35. Hogg D, Pell G, Dupree P, Goubet F, Martín-Orúe SM, Armand S, Gilbert HJ. 2003. The modular architecture of Cellvibrio japonicus mannanases in glycoside hydrolase families 5 and 26 points to differences in their role in mannan degradation. Biochem J 371:1027-1043. http://dx.doi.org/10.1042/BJ20021860.
36. Zhang X, Rogowski A, Zhao L, Hahn MG, Avci U, Knox JP, Gilbert HJ. 2014. Understanding how the complex molecular architecture of mannan-degrading hydrolases contributes to plant cell wall degradation. J Biol Chem 289:2002-2012. http://dx.doi.org/10.1074/jbc.M113.527770.
37. McNulty NP, Wu M, Erickson AR, Pan C, Erickson BK, Martens EC, Pudlo NA, Muegge BD, Henrissat B, Hettich RL, Gordon JI. 2013. Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome. PLoS Biol 11:e1001637. http://dx.doi.org/10.1371/journal.pbio.1001637.