Regulated expression of polysaccharide utilization and capsular biosynthesis loci in biofilm and planktonic Bacteroides thetaiotaomicron during growth in chemostats
dc.contributor.author | TerAvest, Michaela A. | en_US |
dc.contributor.author | He, Zhen | en_US |
dc.contributor.author | Rosenbaum, Miriam A. | en_US |
dc.contributor.author | Martens, Eric C. | en_US |
dc.contributor.author | Cotta, Michael A. | en_US |
dc.contributor.author | Gordon, Jeffrey I. | en_US |
dc.contributor.author | Angenent, Largus T. | en_US |
dc.date.accessioned | 2013-12-04T18:58:10Z | |
dc.date.available | 2015-03-02T14:35:34Z | en_US |
dc.date.issued | 2014-01 | en_US |
dc.identifier.citation | TerAvest, Michaela A.; He, Zhen; Rosenbaum, Miriam A.; Martens, Eric C.; Cotta, Michael A.; Gordon, Jeffrey I.; Angenent, Largus T. (2014). "Regulated expression of polysaccharide utilization and capsular biosynthesis loci in biofilm and planktonic Bacteroides thetaiotaomicron during growth in chemostats." Biotechnology and Bioengineering 111(1): 165-173. | en_US |
dc.identifier.issn | 0006-3592 | en_US |
dc.identifier.issn | 1097-0290 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/101871 | |
dc.description.abstract | Bacteroides thetaiotaomicron is a prominent member of the human distal gut microbiota that specializes in breaking down diet and host‐derived polysaccharides. While polysaccharide utilization has been well studied in B. thetaiotaomicron , other aspects of its behavior are less well characterized, including the factors that allow it to maintain itself in the gut. Biofilm formation may be a mechanism for bacterial retention in the gut. Therefore, we used custom GeneChips to compare the transcriptomes of biofilm and planktonic B. thetaiotaomicron during growth in mono‐colonized chemostats. We identified 1,154 genes with a fold‐change greater than 2, with confidence greater than or equal to 95%. Among the prominent changes observed in biofilm populations were: (i) greater expression of genes in polysaccharide utilization loci that are involved in foraging of O‐glycans normally found in the gut mucosa; and (ii) regulated expression of capsular polysaccharide biosynthesis loci. Hierarchical clustering of the data with different datasets, which were obtained during growth under a range of conditions in minimal media and in intestinal tracts of gnotobiotic mice, revealed that within this group of differentially expressed genes, biofilm communities were more similar to the in vivo samples than to planktonic cells and exhibited features of substrate limitation. The current study also validates the use of chemostats as an in vitro “gnotobiotic” model to study gene expression of attached populations of this bacterium. This is important to gut microbiota research, because bacterial attachment and the consequences of disruptions in attachment are difficult to study in vivo. Biotechnol. Bioeng. 2014;111: 165–173. © 2013 Wiley Periodicals, Inc. The authors used GeneChips to compare the transcriptomes of biofilm and planktonic populations of the human gut symbiont Bacteroides thetaiotaomicron . The biofilm population showed a relative increase in expression of polysaccharide utilization loci, particularly those involved in host‐derived glycan degradation. Comparison to data from other studies with this organism revealed that these changes made the biofilm population more similar to cells grown in mouse ceca than to cells grown planktonically in vitro. | en_US |
dc.publisher | Wiley Periodicals, Inc. | en_US |
dc.subject.other | Microbiology | en_US |
dc.subject.other | Polysaccharide | en_US |
dc.subject.other | Bacteroides Thetaiotaomicron | en_US |
dc.subject.other | Transcriptomics | en_US |
dc.subject.other | Carbohydrate Metabolism | en_US |
dc.subject.other | Biofilm | en_US |
dc.title | Regulated expression of polysaccharide utilization and capsular biosynthesis loci in biofilm and planktonic Bacteroides thetaiotaomicron during growth in chemostats | en_US |
dc.type | Article | en_US |
dc.rights.robots | IndexNoFollow | en_US |
dc.subject.hlbsecondlevel | Public Health | en_US |
dc.subject.hlbsecondlevel | Statistics and Numeric Data | en_US |
dc.subject.hlbsecondlevel | Natural Resources and Environment | en_US |
dc.subject.hlbsecondlevel | Mathematics | en_US |
dc.subject.hlbsecondlevel | Ecology and Evolutionary Biology | en_US |
dc.subject.hlbsecondlevel | Biological Chemistry | en_US |
dc.subject.hlbtoplevel | Social Sciences | en_US |
dc.subject.hlbtoplevel | Science | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/101871/1/bit24994.pdf | |
dc.identifier.doi | 10.1002/bit.24994 | en_US |
dc.identifier.source | Biotechnology and Bioengineering | en_US |
dc.identifier.citedreference | Macfarlane S, Woodmansey EJ, Macfarlane GT. 2005. Colonization of mucin by human intestinal bacteria and establishment of biofilm communities in a two‐stage continuous culture system. Appl Environ Microbiol 71 ( 11 ): 7483 – 7492. | en_US |
dc.identifier.citedreference | Macfarlane S, Macfarlane GT. 2006. Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut. Appl Environ Microbiol 72 ( 9 ): 6204 – 6211. | en_US |
dc.identifier.citedreference | Stevens J, Blixt O, Glaser L, Taubenberger JK, Palese P, Paulson JC, Wilson IA. 2006. Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 355 ( 5 ): 1143 – 1155. | en_US |
dc.identifier.citedreference | 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 ( 7 ): 1241 – 1252. | en_US |
dc.identifier.citedreference | Sonnenburg JL, Xu J, Leipi DD, Chen C‐H, Westover BP, Weatherford J, Buhler JD, Gordon JI. 2005. Glycan foraging in vivo by an intestine‐adapted bacterial symbiont. Science 307 ( 5717 ): 1955 – 1959. | en_US |
dc.identifier.citedreference | Lindén SK, Sutton P, Karlsson NG, Korolik V, McGuckin MA. 2008b. Mucins in the mucosal barrier to infection. Mucosal Immunol 1 ( 3 ): 183 – 197. | en_US |
dc.identifier.citedreference | Macfarlane S, Dillon JF. 2007. Microbial biofilms in the human gastrointestinal tract. J Appl Microbiol 102 ( 5 ): 1187 – 1196. | en_US |
dc.identifier.citedreference | Tibshirani R, Hastie T, Narasimhan B, Chu G. 2002. Diagnosis of multiple cancer types by shrunken centroids of gene expression. Proc Natl Acad Sci USA 99 ( 10 ): 6567 – 6572. | en_US |
dc.identifier.citedreference | Sonnenburg JL, Angenent LT, Gordon JI. 2004. Getting a grip on things: how do communities of bacterial symbionts become established in our intestine ? Nat Immunol 5 ( 6 ): 569 – 573. | en_US |
dc.identifier.citedreference | Shipman JA, Berleman JE, Salyers AA. 2000. Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J Bacteriol 182 ( 19 ): 5365 – 5372. | en_US |
dc.identifier.citedreference | Reeves AR, Wang GR, Salyers AA. 1997. Characterization of four outer membrane proteins that play a role in utilization of starch by Bacteroides thetaiotaomicron. J Bacteriol 179 ( 3 ): 643 – 649. | en_US |
dc.identifier.citedreference | Reeves AR, D'Elia JN, Frias J, Salyers AA. 1996. A Bacteroides thetaiotaomicron outer membrane protein that is essential for utilization of maltooligosaccharides and starch. J Bacteriol 178 ( 3 ): 823 – 830. | en_US |
dc.identifier.citedreference | Ambort D, van der Post S, Johansson MEV, MacKenzie J, Thomsson E, Krengel U, Hansson GC. 2011. Function of the CysD domain of the gel‐forming MUC2 mucin. Biochem J 436: 61 – 70. | en_US |
dc.identifier.citedreference | Ambort D, Johansson MEV, Gustafsson JK, Nilsson HE, Ermund A, Johansson BR, Koeck PJB, Hebert H, Hansson GC. 2012. Calcium and pH‐dependent packing and release of the gel‐forming MUC2 mucin. Proc Natl Acad Sci USA 109 ( 15 ): 5645 – 5650. | en_US |
dc.identifier.citedreference | Bar H, Booth J, Schifano E, Wells MT. 2010. Laplace approximated EM microarray analysis: An empirical Bayes approach for comparative microarray experiments. Stat Sci 25 ( 3 ): 388 – 407. | en_US |
dc.identifier.citedreference | Beloin C, Ghigo J‐M. 2005. Finding gene‐expression patterns in bacterial biofilms. Trends Microbiol 13 ( 1 ): 16 – 19. | en_US |
dc.identifier.citedreference | Benjdia A, Martens EC, Gordon JI, Berteau O. 2011. Sulfatases and a radical S‐Adenosyl‐l‐methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron. J Biol Chem 286 ( 29 ): 25973 – 25982. | en_US |
dc.identifier.citedreference | Blixt O, Head S, Mondala T, Scanlan C, Huflejt ME, Alvarez R, Bryan MC, Fazio F, Calarese D, Stevens J, Razi N, Stevens DJ, Skehel JJ, van Die I, Burton DR, Wilson IA, Cummings R, Bovin N, Wong CH, Paulson JC. 2004. Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc Natl Acad Sci USA 101 ( 49 ): 17033 – 17038. | en_US |
dc.identifier.citedreference | Edgar R, Domrachev M, Lash AE. 2002. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30 ( 1 ): 207 – 210. | en_US |
dc.identifier.citedreference | Folsom J, Richards L, Pitts B, Roe F, Ehrlich G, Parker A, Mazurie A, Stewart P. 2010. Physiology of Pseudomonas aeruginosa in biofilms as revealed by transcriptome analysis. BMC Microbiol 10 ( 1 ): 294. | en_US |
dc.identifier.citedreference | Kitamura M, Okuyama M, Tanzawa F, Mori H, Kitago Y, Watanabe N, Kimura A, Tanaka I, Yao M. 2008. Structural and functional analysis of a glycoside hydrolase family 97 enzyme from Bacteroides thetaiotaomicron. J Biol Chem 283 ( 52 ): 36328 – 36337. | en_US |
dc.identifier.citedreference | Koropatkin NM, Smith TJ. 2010. SusG: A unique cell‐membrane‐associated α‐amylase from a prominent human gut symbiont targets complex starch molecules. Structure 18 ( 2 ): 200 – 215. | en_US |
dc.identifier.citedreference | 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 ( 7 ): 1105 – 1115. | en_US |
dc.identifier.citedreference | Koropatkin N, Martens EC, Gordon JI, Smith TJ. 2009. Structure of a SusD homologue, BT1043, involved in mucin O‐glycan utilization in a prominent human gut symbiont. Biochemistry 48 ( 7 ): 1532 – 1542. | en_US |
dc.identifier.citedreference | Koropatkin NM, Cameron EA, Martens EC. 2012. How glycan metabolism shapes the human gut microbiota. Nat Rev Microbiol 10 ( 5 ): 323 – 335. | en_US |
dc.identifier.citedreference | Lazazzera BA. 2005. Lessons from DNA microarray analysis: The gene expression profile of biofilms. Curr Opin Microbiol 8 ( 2 ): 222 – 227. | en_US |
dc.identifier.citedreference | Lindén SK, Florin THJ, McGuckin MA. 2008a. Mucin dynamics in intestinal bacterial infection. PLoS ONE 3 ( 12 ): e3952. | en_US |
dc.identifier.citedreference | Padler‐Karavani V, Song XZ, Yu H, Hurtado‐Ziola N, Huang SS, Muthana S, Chokhawala HA, Cheng JS, Verhagen A, Langereis MA, Kleene R, Schachner M, de Groot RJ, Lasanajak Y, Matsuda H, Schwab R, Chen X, Smith DF, Cummings RD, Varki A. 2012. Cross‐comparison of protein recognition of sialic acid diversity on two novel sialoglycan microarrays. J Biol Chem 287 ( 27 ): 22593 – 22608. | en_US |
dc.identifier.citedreference | McGuckin MA, Lindén SK, Sutton P, Florin TH. 2011. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9 ( 4 ): 265 – 278. | en_US |
dc.identifier.citedreference | Marzorati M, Van den Abbeele P, Possemiers S, Benner J, Verstraete W, Van de Wiele T. 2011. Studying the host‐microbiota interaction in the human gastrointestinal tract: Basic concepts and in vitro approaches. Ann Microbiol 61 ( 4 ): 709 – 715. | en_US |
dc.identifier.citedreference | 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 ( 12 ): e1001221. | en_US |
dc.identifier.citedreference | Martens EC, Roth R, Heuser JE, Gordon JI. 2009. Coordinate regulation of glycan degradation and polysaccharide capsule biosynthesis by a prominent human gut symbiont. J Biol Chem 284 ( 27 ): 18445 – 18457. | en_US |
dc.identifier.citedreference | Martens EC, Chiang HC, Gordon JI. 2008. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 4 ( 5 ): 447 – 457. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.