Microbiology and Biotechnology Letters (한국미생물·생명공학회지)

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Challenging the Hypothesis of de novo Biosynthesis of Bile Acids by Marine Bacteria

  • Tueros, Felipe Gonzalo (Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark) ;
  • Ellabaan, Mostafa M. Hashim (Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark) ;
  • Henricsson, Marcus (Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital) ;
  • Vazquez-Uribe, Ruben (Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark) ;
  • Backhed, Fredrik (Department of Molecular and Clinical Medicine/Wallenberg Laboratory, Institute of Medicine, University of Gothenburg and Sahlgrenska University Hospital) ;
  • Sommer, Morten Otto Alexander (Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark)
  • Received : 2021.11.16
  • Accepted : 2022.01.19
  • Published : 2022.03.28
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Abstract

Bile acids are essential molecules produced by vertebrates that are involved in several physiological roles, including the uptake of nutrients. Bacterial isolates capable of producing bile acids de novo have been identified and characterized. Such isolates may provide access to novel biochemical pathways suitable for the design of microbial cell factories. Here, we further characterized the ability of Maribacter dokdonensis, Dokdonia donghaensis, and Myroides pelagicus to produce bile acids. Contrary to previous reports, we did not observe de novo production of bile acids by these isolates. Instead, we found that these isolates deconjugated the amino acid moiety of bile acids present in the growth medium used in previous reports. Through genomic analysis, we identified putative bile salt hydrolases, which could be responsible for the different bile acid modifications observed. Our results challenge the hypothesis of de novo microbial bile acid production, while further demonstrating the diverse capacity of bacteria to modify bile acids.

Keywords

Acknowledgement

This research was funded by The Novo Nordisk Foundation under NNF grant number: NNF20CC0035580; and The Novo Nordisk Foundation, Challenge programme, CaMiT under grant agreement: NNF17-CO0028232. F.G.T. also acknowledges NNF PhD fellowship grant no. NNF16CC0020908. M.O.A.S. acknowledges additional funding from the NNF.

References

  1. Hofmann AF, Hagey LR, Krasowski MD. 2010. Bile salts of vertebrates: structural variation and possible evolutionary significance. J. Lipid Res. 51: 226-246. https://doi.org/10.1194/jlr.R000042
  2. Hofmann AF, Hagey LR. 2008. Review bile acids: Chemistry, pathochemistry, biology, pathobiology, and therapeutics. Cell. Mol. Life Sci. 65: 2461-2483. https://doi.org/10.1007/s00018-008-7568-6
  3. Foley MH, Flaherty SO, Barrangou R, Theriot CM. 2019. Bile salt hydrolases: Gatekeepers of bile acid metabolism and host-microbiome crosstalk in the gastrointestinal tract. PLoS Pathog. 15: e1007581. https://doi.org/10.1371/journal.ppat.1007581
  4. Jones BV, Begley M, Hill C, Gahan CGM, Marchesi JR. 2008. Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc. Natl. Acad. Sci. USA 105: 13580-13585. https://doi.org/10.1073/pnas.0804437105
  5. Russell DW, Setchell KDR. 1992. Bile acid biosynthesis. Biochemistry 31: 4737-4749. https://doi.org/10.1021/bi00135a001
  6. Hofmann AF. 1999. The continuing importance of bile acids in liver and intestinal disease. Arch. Intern. Med. 159: 2647-2658. https://doi.org/10.1001/archinte.159.22.2647
  7. Bowlus CL. 2016. Obeticholic acid for the treatment of primary biliary cholangitis in adult patients: clinical utility and patient selection. Hepat. Med. 8: 89-95. https://doi.org/10.2147/HMER.S91709
  8. Kim DJ, Yoon S, Ji SC, Yang J, Kim YK, Lee S, et al. 2018. Ursodeoxycholic acid improves liver function via phenylalanine/tyrosine pathway and microbiome remodelling in patients with liver dysfunction. Sci. Rep. 8: 11874. https://doi.org/10.1038/s41598-018-30349-1
  9. Passed A, Lang S, Wagner F, Wray V. 1991. Anionic trehalose tetraester from the marine bacterium Arthrobacter sp. EK 1. Naturforsch 46c: 204-209.
  10. Maneerat S, Nitoda T, Kanzaki H, Kawai F. 2005. Bile acids are new products of a marine bacterium, Myroides sp. strain SM1. Appl. Microbiol. Cell Physiol. 67: 679-683.
  11. Kim D, Kim J, Kang SJ, Yoon JH, Kim WG, Lee JS, et al. 2007. Biosynthesis of bile acids in a variety of marine bacteria taxa. J. Microbiol. Biotechnol. 17: 403-407.
  12. Tremaroli V, Karlsson F, Werling M, Stahlman M, KovatchevaDatchary P, Olbers T, et al. 2015. Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab. 22: 228-238. https://doi.org/10.1016/j.cmet.2015.07.009
  13. Tatusov RL, Galperin MY, Natale DA, Koonin EV. 2000. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 28: 33-36. https://doi.org/10.1093/nar/28.1.33
  14. Besemer J, Lomsadze A, Borodovsky M. 2001. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res. 29: 2607-2618. https://doi.org/10.1093/nar/29.12.2607
  15. Madeira F, Park YM, Lee J, Buso N, Gur T, Madhusoodanan N, et al. 2019. The EMBL-EBI search and sequence analysis tools APIs in 2019. Nucleic Acids Res. 47: W636-W641. https://doi.org/10.1093/nar/gkz268
  16. Price MN, Dehal PS, Arkin AP. 2009. FastTree: Computing large minimum-evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26: 1641-1650. https://doi.org/10.1093/molbev/msp077
  17. Ohashi K, Miyagawa Y, Nakamura Y, Shibuya H. 2008. Bioproduction of bile acids and the glycine conjugates by Penicillium fungus. J. Nat. Med. 62: 83-86. https://doi.org/10.1007/s11418-007-0190-3
  18. Park SC, Kim CJ, Uramoto M, Yun HI, Yoon KH, Oh TK. 1995. Antibacterial substance produced by Streptococcus faecium under anaerobic culture. Biosci. Biotechnol. Biochem. 59: 1966-1967. https://doi.org/10.1271/bbb.59.1966
  19. Hill C, Gahan CGM. 2006. Bile salt hydrolase activity in probiotics. Appl. Environ. Microbiol. 72: 1729-1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006
  20. Panigrahi P, Sule M, Sharma R, Ramasamy S, Suresh, CG. 2014. An improved method for specificity annotation shows a distinct evolutionary divergence among the microbial enzymes of the cholylglycine hydrolase family. Microbiology 160: 1162-1174. https://doi.org/10.1099/mic.0.077586-0
  21. Valle F, Balbas P, Merino E, Bollvar F. 1991. The role of penicillin amidases in nature and in industry. Trends Biochem. Sci. 16: 36-40. https://doi.org/10.1016/0968-0004(91)90014-M
  22. Kim SH, Yang HO, Sohn YC, Kwon HC. 2010. Aeromicrobium halocynthiae sp. nov., a taurocholic acid-producing bacterium isolated from the marine ascidian Halocynthia roretzi. Int. J. Syst. Evol. Microbiol. 60: 2793-2798. https://doi.org/10.1099/ijs.0.016618-0
  23. Li H, Shinde PB, Lee HJ, Yoo ES, Hong J, Choi SH, et al. 2009. Bile acid derivatives from a sponge-associated bacterium. Arch. Pharm. Res. 32: 857-862. https://doi.org/10.1007/s12272-009-1607-1
  24. Kim SH, Yang HO, Shin YK, Kwon HC. 2012. Hasllibacter halocynthiae gen. nov., sp. nov., a nutriacholic acid-producing bacterium isolated from the marine ascidian Halocynthia roretzi. Int. J. Syst. Evol. Microbiol. 62: 624-631. https://doi.org/10.1099/ijs.0.028738-0