Formate cross-feeding and cooperative metabolic interactions revealed by transcriptomics in co-cultures of acetogenic and amylolytic human colonic bacteria

Environmental Microbiology

Volumn 21, Issue 1, 2019, Pages 259-271

  Laverde Gomez, Jenny A ^a   Mukhopadhya, Indrani ^a   Duncan, Sylvia H ^a   Louis, Petra ^a   Shaw, Sophie ^b   Collie Duguid, Elaina ^b   Crost, Emmanuelle ^c   Juge, Nathalie ^c   Flint, Harry J ^a  

^a ROWETT RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ALCOHOL; FORMIC ACID DERIVATIVE; STARCH; TRANSCRIPTOME;

BACTERIUM; COCULTURE; COLON; FERMENTATION; HUMAN; METABOLISM; MICROBIOLOGY; ORGANISMAL INTERACTION; PHYSIOLOGY; RUMINOCOCCUS;

ACETATES; BACTERIA; COCULTURE TECHNIQUES; COLON; ETHANOL; FERMENTATION; FORMATES; HUMANS; MICROBIAL INTERACTIONS; RUMINOCOCCUS; STARCH; TRANSCRIPTOME;

EID: 85057008696     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.14454     Document Type: Article

References (42)

1. Anders, S., and Huber, W. (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
2. Anders, S., Pyl, P. T., and Huber, W. (2015) HTSeq—a python framework to work with high-throughput sequencing data. Bioinformatics 31: 166–169.
3. Barcenilla, A., Pryde, S. E., Martin, J. C., Duncan, S. H., Stewart, C. S., Henderson, C., and Flint, H. J. (2000) Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66: 1654–1661.
4. Bernalier, A., Willems, A., Leclerc, M., Rochet, V., and Collins, M. D. (1996) Ruminococcus hydrogenotrophicus sp. nov., a new H2/CO2-utilizing acetogenic bacterium isolated from human feces. Arch Microbiol 166: 176–183.
5. Chassard, C., and Bernalier-Donadille, A. (2005) H2 and acetate transfers during xylan fermentation between a butyrate-producing xylanolytic species and hydrogenotrophic microorganisms from the human gut. FEMS Microbiol Lett 254: 116–122.
6. Chung, W. S., Walker, A. W., Louis, P., Parkhill, J., Vermeiren, J., Bosscher, D., et al. (2016) Modulation of the human gut microbiota by dietary fibres occurs at the species level. BMC Biol 14: 3.
7. Costliow, Z. A., and Degnan, P. H. (2017) Thiamine acquisition strategies impact metabolism and competition in the gut microbe Bacteroides thetaiotaomicron. MSystems 2: e00116–e00117.
8. Doré, J., Pochart, P., Bernalier, A., Goderel, I., Morvan, B., and Rambaud, J. (1995) Enumeration of H2-utilizing methanogenic archaea, acetogenic and sulfate-reducing bacteria from human feces. FEMS Microbiol Ecol 17: 279–284.
9. Du, Q., Wang, H., and Xie, J. (2011) Thiamin (vitamin B1) biosynthesis and regulation: a rich source of antimicrobial drug targets? Int J Biol Sci 7: 41.
10. Dubois, M., Gilles, K., Hamilton, J., Rebers, P., and Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350–356.
11. Florin, T. H., Zhu, G., Kirk, K. M., and Martin, N. G. (2000) Shared and unique environmental factors determine the ecology of methanogens in humans and rats. Am J Gastroenterol 95: 2872.
12. Herbeck, J. L., and Bryant, M. (1974) Nutritional features of the intestinal anaerobe Ruminococcus bromii. Appl Microbiol 28: 1018–1022.
13. Hochberg, Y., and Benjamini, Y. (1990) More powerful procedures for multiple significance testing. Stat Med 9: 811–818.
14. Kamlage, B., Gruhl, B., and Blaut, M. (1997) Isolation and characterization of two new homoacetogenic hydrogen-utilizing bacteria from the human intestinal tract that are closely related to Clostridium coccoides. Appl Environ Microbiol 63: 1732–1738.
15. Kettle, H., Louis, P., Holtrop, G., Duncan, S. H., and Flint, H. J. (2015) Modelling the emergent dynamics and major metabolites of the human colonic microbiota. Environ Microbiol 17: 1615–1630.
16. Leclerc, M., Bernalier, A., Donadille, G., and Lelait, M. (1997) H 2/CO 2 metabolism in acetogenic bacteria isolated from the human colon. Anaerobe 3: 307–315.
17. Lever, M. (1977) Carbohydrate determination with 4-hydroxybenzoic acid hydrazide (PAHBAH): effect of bismuth on the reaction. Anal Biochem 81: 21–27.
18. Louis, P., and Flint, H. J. (2017) Formation of propionate and butyrate by the human colonic microbiota. Environ Microbiol 19: 29–41.
19. Macfarlane, G. T., and Gibson, G. R. (1997) Carbohydrate fermentation, energy transduction and gas metabolism in the human large intestine. In Gastrointestinal Microbiology, Mackie, R. L., and White, B. A. (eds). Boston, MA: Springer, pp. 269–318.
20. Magnúsdóttir, S., Ravcheev, D., de Crécy-Lagard, V., and Thiele, I. (2015) Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front Genet 6: 148.
21. Martínez, I., Kim, J., Duffy, P. R., Schlegel, V. L., and Walter, J. (2010) Resistant starches types 2 and 4 have differential effects on the composition of the fecal microbiota in human subjects. PLoS One 5: e15046.
22. Miyazaki, K., Martin, J. C., Marinsek-Logar, R., and Flint, H. J. (1997) Degradation and utilization of xylans by the rumen anaerobe Prevotella bryantii (formerly P. ruminicola subsp. brevis) B(1)4. Anaerobe 3: 373–381.
23. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A. C., and Kanehisa, M. (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182–W185.
24. Mukhopadhya, I., Moraïs, S., Laverde-Gomez, J., Sheridan, P. O., Walker, A. W., Kelly, W., et al. (2018) Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch-degrader Ruminococcus bromii. Environ Microbiol 20: 324–336.
25. Rasmussen, H. S., Holtug, K., and Mortensen, P. (1988) Degradation of amino acids to short-chain fatty acids in humans: an in vitro study. Scand J Gastroenterol 23: 178–182.
26. Rey, F. E., Faith, J. J., Bain, J., Muehlbauer, M. J., Stevens, R. D., Newgard, C. B., and Gordon, J. I. (2010) Dissecting the in vivo metabolic potential of two human gut acetogens. J Biol Chem 285: 22082–22090.
27. Richardson, A., Calder, A., Stewart, C., and Smith, A. (1989) Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography. Lett Appl Microbiol 9: 5–8.
28. Rodionov, D. A., Vitreschak, A. G., Mironov, A. A., and Gelfand, M. S. (2002) Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J Biol Chem 277: 48949–48959.
29. Rückert, C. (2016) Sulfate reduction in microorganisms—recent advances and biotechnological applications. Curr Opin Microbiol 33: 140–146.
30. Sander, K., Wilson, C. M., Rodriguez, M., Klingeman, D. M., Rydzak, T., Davison, B. H., and Brown, S. D. (2015) Clostridium thermocellum DSM 1313 transcriptional responses to redox perturbation. Biotechnol Biofuels 8: 211.
31. Sieber, J. R., McInerney, M. J., and Gunsalus, R. P. (2012) Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66: 429–452.
32. Stroupe, M. E., Leech, H. K., Daniels, D. S., Warren, M. J., and Getzoff, E. D. (2003) CysG structure reveals tetrapyrrole-binding features and novel regulation of siroheme biosynthesis. Nat Struct Mol Biol 10: 1064.
33. Trapnell, C., Pachter, L., and Salzberg, S. L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.
34. Wagner, M., Roger, A. J., Flax, J. L., Brusseau, G. A., and Stahl, D. A. (1998) Phylogeny of dissimilatory sulfite reductases supports an early origin of sulfate respiration. J Bacteriol 180: 2975–2982.
35. Walker, A. W., Ince, J., Duncan, S. H., Webster, L. M., Holtrop, G., Ze, X., et al. (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J 5: 220–230.
36. Whitman, W. B., Coleman, D. C., and Wiebe, W. J. (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95: 6578–6583.
37. Wolf, P. G., Biswas, A., Morales, S. E., Greening, C., and Gaskins, H. R. (2016) H2 metabolism is widespread and diverse among human colonic microbes. Gut microbes 7: 235–245.
38. Wolin, M., Miller, T., and Stewart, C. (1997)Microbe-microbe interactions. In The Rumen Microbial Ecosystem. London, UK: Springer, pp. 467–491.
39. Wolin, M. J., Miller, T. L., Collins, M. D., and Lawson, P. A. (2003) Formate-dependent growth and homoacetogenic fermentation by a bacterium from human feces: description of Bryantella formatexigens gen. Nov., sp. nov. Appl Environ Microbiol 69: 6321–6326.
40. Wolin, M. J., Miller, T. L., Yerry, S., Zhang, Y., Bank, S, and Weaver, G. A. (1999) Changes of fermentation pathways of fecal microbial communities associated with a drug treatment that increases dietary starch in the human colon. Appl Environ Microbiol 65: 2807–2812.
41. Ze, X., Duncan, S. H., Louis, P., and Flint, H. J. (2012) Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J 6: 1535–1543.
42. Ze, X., Ben David, Y., Laverde-Gomez, J. A., Dassa, B., Sheridan, P. O., Duncan, S. H., et al. (2015) Unique organization of extracellular amylases into amylosomes in the resistant starch-utilizing human colonic Firmicutes bacterium Ruminococcus bromii. MBio 6: e01058–e01015.