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Volume 166, Issue 7

Nutrient-dependent morphological variability of Free

Abstract

Unique morphologies can enable bacteria to survive in their native environment. Furthermore, many bacteria change their cell shape to adapt to different environmental conditions. For instance, some bacteria increase their surface area under carbon or nitrogen starvation. is an abundant human gut species; it efficiently degrades a number of carbohydrates and also supports the growth of other bacteria by breaking down complex polysaccharides. The gut provides a variable environment as nutrient availability is subject to the diet and health of the host, yet how gut bacteria adapt and change their morphologies under different nutrient conditions has not been studied. Here, for the first time, we report an elongated morphology under sugar-limited conditions using live-cell imaging; this elongated morphology is enhanced in the presence of sodium bicarbonate. Similarly, we also observed that sodium bicarbonate produces an elongated-length phenotype in another Gram-negative gut bacterium, . The increase in cell length might provide an adaptive advantage for cells to survive under nutrient-limited conditions.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): elongated phenotype , microbiome , sodium bicarbonate and sugar-limited
Funding
This study was supported by the:
  • Army Research Office (Award W911NF‐18‐1‐0339)
    • Principle Award Recipient: Julie Biteen
© 2020 The Authors
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2020-05-14
2024-04-16
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References

  1. Kysela DT, Randich AM, Caccamo PD, Brun YV. Diversity takes shape: understanding the mechanistic and adaptive basis of bacterial morphology. PLoS Biol 2016; 14:e1002565–15 [View Article][PubMed]
     [Google Scholar]
  2. Yang DC, Blair KM, Salama NR. Staying in shape: the impact of cell shape on bacterial survival in diverse environments. Microbiol Mol Biol Rev 2016; 80:187–203 [View Article][PubMed]
     [Google Scholar]
  3. Young KD. Bacterial morphology: why have different shapes?. Curr Opin Microbiol 2007; 10:596–600 [View Article][PubMed]
     [Google Scholar]
  4. Jun S, Si F, Pugatch R, Scott M. Fundamental principles in bacterial physiology-history, recent progress, and the future with focus on cell size control: a review. Rep Prog Phys 2018; 81:056601 [View Article][PubMed]
     [Google Scholar]
  5. Sargent MG. Control of cell length in Bacillus subtilis . J Bacteriol 1975; 123:7–19 [View Article][PubMed]
     [Google Scholar]
  6. Steinberger RE, Allen AR, Hansa HG, Holden PA. Elongation correlates with nutrient deprivation in Pseudomonas aeruginosa-unsaturates biofilms. Microb Ecol 2002; 43:416–423 [View Article][PubMed]
     [Google Scholar]
  7. Gonin M, Quardokus EM, O'Donnol D, Maddock J, Brun YV. Regulation of stalk elongation by phosphate in Caulobacter crescentus . J Bacteriol 2000; 182:337–347 [View Article][PubMed]
     [Google Scholar]
  8. Sycuro LK, Pincus Z, Gutierrez KD, Biboy J, Stern CA et al. Peptidoglycan crosslinking relaxation promotes Helicobacter pylori's helical shape and stomach colonization. Cell 2010; 141:822–833 [View Article][PubMed]
     [Google Scholar]
  9. Kieser KJ, Rubin EJ. How sisters grow apart: mycobacterial growth and division. Nat Rev Microbiol 2014; 12:550–562 [View Article][PubMed]
     [Google Scholar]
  10. Distaso A. Contribution l'étude sur l'intoxication intestinale. Centralbl Bakteriol Parasit Orig 1912; 62:433–468
     [Google Scholar]
  11. Ding T, Schloss PD. Dynamics and associations of microbial community types across the human body. Nature 2014; 509:357–360 [View Article][PubMed]
     [Google Scholar]
  12. El Kaoutari A, Armougom F, Gordon JI, Raoult D, Henrissat B. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat Rev Microbiol 2013; 11:497–504 [View Article][PubMed]
     [Google Scholar]
  13. Martens EC, Chiang HC, Gordon JI. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 2008; 4:447–457 [View Article]
     [Google Scholar]
  14. Schwalm ND, Townsend GE, Groisman EA. Prioritization of polysaccharide utilization and control of regulator activation in Bacteroides thetaiotaomicron . Mol Microbiol 2017; 104:32–45 [View Article][PubMed]
     [Google Scholar]
  15. Rakoff-Nahoum S, Coyne MJ, Comstock LE. An ecological network of polysaccharide utilization among human intestinal symbionts. Curr Biol 2014; 24:40–49 [View Article][PubMed]
     [Google Scholar]
  16. Rakoff-Nahoum S, Foster KR, Comstock LE. The evolution of cooperation within the gut microbiota. Nature 2016; 533:255–259 [View Article][PubMed]
     [Google Scholar]
  17. Ze X, Duncan SH, Louis P, Flint HJ. Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon. ISME J 2012; 6:1535–1543 [View Article][PubMed]
     [Google Scholar]
  18. Ze X, Ben David Y, Laverde-Gomez JA, Dassa B, Sheridan PO et al. Unique Organization of Extracellular Amylases into Amylosomes in the Resistant Starch-Utilizing Human Colonic Firmicutes Bacterium Ruminococcus bromii . mBio 2015; 6:1–11 [View Article][PubMed]
     [Google Scholar]
  19. Holwerda EK, Hirst KD, Lynd LR. A defined growth medium with very low background carbon for culturing Clostridium thermocellum . J Ind Microbiol Biotechnol 2012; 39:943–947 [View Article][PubMed]
     [Google Scholar]
  20. Thompson KA, Summers RS, Cook SM. Development and experimental validation of the composition and treatability of a new synthetic bathroom greywater (SynGrey). Environ Sci Water Res Technol 2017; 3:1120–1131 [View Article]
     [Google Scholar]
  21. Dobay O, Laub K, Stercz B, Kéri A, Balázs B et al. Bicarbonate inhibits bacterial growth and biofilm formation of prevalent cystic fibrosis pathogens. Front Microbiol 2018; 9:1–12 [View Article]
     [Google Scholar]
  22. Jarvis GN, Fields MW, Adamovich DA, Arthurs CE, Russell JB. The mechanism of carbonate killing of Escherichia coli . Lett Appl Microbiol 2001; 33:196–200 [View Article][PubMed]
     [Google Scholar]
  23. Murakami S, Goto Y, Ito K, Hayasaka S, Kurihara S et al. The consumption of Bicarbonate-Rich mineral water improves glycemic control. Evid Based Complement Alternat Med 2015; 2015:1–10 [View Article][PubMed]
     [Google Scholar]
  24. Bacic MK, Smith CJ. Laboratory maintenance and cultivation of Bacteroides species. Curr Protoc Microbiol 2008; Chapter 13:13C.1.1–13.113 [View Article][PubMed]
     [Google Scholar]
  25. Lassiter JW, Hamdy MK, Buranamanas P. Effect of sodium bicarbonate on microbial activity in the rumen. J Anim Sci 1963; 22:335–340 [View Article]
     [Google Scholar]
  26. Hopfer U, Liedtke CM. Proton and bicarbonate transport mechanisms in the intestine. Annu Rev Physiol 1987; 49:51–67 [View Article][PubMed]
     [Google Scholar]
  27. Carter MJ, Parsons DS. The isoenzymes of carbonic anhydrase: tissue, subcellular distribution and functional significance, with particular reference to the intestinal tract. J Physiol 1971; 215:71–94 [View Article][PubMed]
     [Google Scholar]
  28. Macy JM, Probst I. The biology of gastrointestinal Bacteroides . Annu Rev Microbiol 1979; 33:561–594 [View Article][PubMed]
     [Google Scholar]
  29. Macy JM, Ljungdahl LG, Gottschalk G. Pathway of succinate and propionate formation in Bacteroides fragilis . J Bacteriol 1978; 134:84–91 [View Article][PubMed]
     [Google Scholar]
  30. Caspari D, Macy JM. The role of carbon dioxide in glucose metabolism of Bacteroides fragilis . Arch Microbiol 1983; 135:16–24 [View Article][PubMed]
     [Google Scholar]
  31. Rey FE, Faith JJ, Bain J, Muehlbauer MJ, Stevens RD et al. Dissecting the in vivo metabolic potential of two human gut acetogens. J Biol Chem 2010; 285:22082–22090 [View Article][PubMed]
     [Google Scholar]
  32. Fischbach MA, Sonnenburg JL. Eating for two: how metabolism establishes interspecies interactions in the gut. Cell Host Microbe 2011; 10:336–347 [View Article][PubMed]
     [Google Scholar]
  33. Hansen TH, Thomassen MT, Madsen ML, Kern T, Bak EG et al. The effect of drinking water pH on the human gut microbiota and glucose regulation: results of a randomized controlled cross-over intervention. Sci Rep 2018; 8:1–12 [View Article]
     [Google Scholar]
  34. Mahowald MA, Rey FE, Seedorf H, Turnbaugh PJ, Fulton RS et al. Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla. Proc Natl Acad Sci U S A 2009; 106:5859–5864 [View Article]
     [Google Scholar]
  35. Holdeman L V, Moore WEC. Anaerobe Laboratory Manual, by the Staff of the Anaerobe Laboratory, Virginia Polytechnic Institute and State University Blacksburg: V.P.I. Anaerobe Laboratory; 1973
     [Google Scholar]
  36. Martens EC, Chiang HC, Gordon JI. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 2008; 4:447–457 [View Article][PubMed]
     [Google Scholar]
  37. Miller JH. A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harb Lab Press Cold Spring Harb; 1992
     [Google Scholar]
  38. Karunatilaka KS, Cameron EA, Martens EC, Koropatkin NM, Biteen JS. Superresolution imaging captures carbohydrate utilization dynamics in human gut symbionts. mBio 2014; 5:1–10 [View Article][PubMed]
     [Google Scholar]
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Nutrient-dependent morphological variability of Bacteroides thetaiotaomicron
Microbiology 166, 624 (2020); https://doi.org/10.1099/mic.0.000924
/content/journal/micro/10.1099/mic.0.000924
/content/journal/micro/10.1099/mic.0.000924
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