1887

Abstract

Many microorganisms engaged in host-microbe interactions pendulate between a free-living phase and a host-affiliated stage. How adaptation to stress during the free-living phase affects host-microbe associations is unclear and understudied. To explore this topic, the symbiosis between Hawaiian bobtail squid () and the luminous bacterium was leveraged for a microbial experimental evolution study. experienced adaptation to extreme pH while apart from the squid host. was serially passaged for 2000 generations to the lower and upper pH growth limits for this microorganism, which were pH 6.0 and 10.0, respectively. was also serially passaged for 2000 generations to vacillating pH 6.0 and 10.0. Evolution to pH stress both facilitated and impaired symbiosis. Microbial evolution to acid stress promoted squid colonization and increased bioluminescence for , while symbiont adaptation to alkaline stress diminished these two traits. Oscillatory selection to acid and alkaline stress also improved symbiosis for , but the facilitating effects were less than that provided by microbial adaptation to acid stress. In summary, microbial adaptation to harsh environments amid the free-living phase may impact the evolution of host-microbe interactions in ways that were not formerly considered.

Funding
This study was supported by the:
  • College of William and Mary Startup (Award 120819)
    • Principle Award Recipient: William Soto
  • College of William and Mary Startup (Award 121089)
    • Principle Award Recipient: William Soto
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000884
2020-01-22
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/166/3/262.html?itemId=/content/journal/micro/10.1099/mic.0.000884&mimeType=html&fmt=ahah

References

  1. Soto W, Lostroh CP, Nishiguchi MK. Physiological responses to stress in the Vibrionaceae. In Seckback J, Grube M. (editors) Symbiosis and Stress: Joint Ventures in Biology New York City, New York, United States of America: Springer; 2010 pp 407–426
    [Google Scholar]
  2. Marles-Wright J, Lewis RJ. Stress responses of bacteria. Curr Opin Struct Biol 2007; 17:755–760 [View Article]
    [Google Scholar]
  3. White D, Drummond J, Clay Fuqua C. The Physiology and Biochemistry of Prokaryotes, 4th edn. Oxford, United Kingdom: Oxford University Press; 2011
    [Google Scholar]
  4. Atlas RM, Bartha R. Microbial Ecology: Fundamentals and Applications, 4th edn. Menlo Park, California, United States of America: Benjamin Cummings; 1998
    [Google Scholar]
  5. Leung TLF, Poulin R. Parasitism, commensalism, and mutualism: exploring the many shades of symbioses. Vie et Milieu 2008; 58:107–115
    [Google Scholar]
  6. Faruque SM, Nair GB, Mekalanos JJ. Genetics of stress adaptation and virulence in toxigenic Vibrio cholerae . DNA Cell Biol 2004; 23:723–741 [View Article][PubMed]
    [Google Scholar]
  7. Gophna U, Ron EZ. Virulence and the heat shock response. Int J Med Microbiol 2003; 292:453–461 [View Article][PubMed]
    [Google Scholar]
  8. Labidi M, Laberge S, Vézina LP, Antoun H. The dnaJ (Hsp40) locus in Rhizobium leguminosarum bv. phaseoli is required for the establishment of an effective symbiosis with Phaseolus vulgaris . Mol Plant Microbe Interact 2000; 13:1271–1274 [View Article][PubMed]
    [Google Scholar]
  9. Soto W, Punke EB, Nishiguchi MK. Evolutionary perspectives in a mutualism of sepiolid squid and bioluminescent bacteria: combined usage of microbial experimental evolution and temporal population genetics. Evolution 2012; 66:1308–1321 [View Article]
    [Google Scholar]
  10. Nishiguchi MK EG, Ruby EG, McFall-Ngai MJ. Competitive dominance during colonization is an indicator of coevolution in an animal-bacterial symbiosis. Applied and Environmental Microbiology 1998; 64:3209–3213
    [Google Scholar]
  11. Jereb P, Roper CFE. Cephalopods of the World: Chambered Nautiluses and Sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae, and Spirulidae) Rome, Italy: Food and Agriculture Organization of the United Nations; 2005
    [Google Scholar]
  12. Jones BW, Nishiguchi MK. Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes berry (Mollusca: Cephalopoda). Mar Biol 2004; 144:1151–1155 [View Article]
    [Google Scholar]
  13. Johnsen S, Widder EA, Mobley CD. Propagation and perception of bioluminescence: factors affecting counterillumination as a cryptic strategy. Biol Bull 2004; 207:1–16 [View Article]
    [Google Scholar]
  14. Latz MI. Physiological mechanisms in the control of bioluminescent countershading in a midwater shrimp. Mar Freshw Behav Physiol 1995; 26:207–218 [View Article]
    [Google Scholar]
  15. McFall-Ngai M. Divining the essence of symbiosis: insights from the squid-Vibrio model. PLoS Biol 2014; 12:e1001783 [View Article]
    [Google Scholar]
  16. Soto W, Gutierrez J, Remmenga MD, Nishiguchi MK. Salinity and temperature effects on physiological responses of Vibrio fischeri from diverse ecological niches. Microb Ecol 2009; 57:140–150 [View Article]
    [Google Scholar]
  17. Wollenberg MS, Preheim SP, Polz MF, Ruby EG. Polyphyly of non-bioluminescent Vibrio fischeri sharing a lux-locus deletion. Environ Microbiol 2012; 14:655–668 [View Article]
    [Google Scholar]
  18. Soto W, Nishiguchi MK. Microbial experimental evolution as a novel research approach in the Vibrionaceae and squid-Vibrio symbiosis. Front Microbiol 2014; 5:593 [View Article]
    [Google Scholar]
  19. Tazi L, Breakwell DP, Harker AR, Crandall KA. Life in extreme environments: microbial diversity in Great Salt Lake, Utah. Extremophiles 2014; 18:525–535 [View Article]
    [Google Scholar]
  20. Jacob JH, Hussein EI, Shakhatreh MAK, Cornelison CT. Microbial community analysis of the hypersaline water of the Dead Sea using high-throughput amplicon sequencing. Microbiologyopen 2017; 6:e00500 [View Article]
    [Google Scholar]
  21. Urakawa H, Rivera ING. Aquatic environments. In Thompson FL, Austin B, Swings J. (editors) Biology of Vibrios Washington, D.C: ASM Press; 2006
    [Google Scholar]
  22. Thompson FL, Austin B, Swings JG. (editors) Adaptive responses of vibrios. The Biology of Vibrios Washington, DC, United States of America: ASM Press; 2006
    [Google Scholar]
  23. Lutz C, Erken M, Noorian P, Sun S, McDougald D. Environmental reservoirs and mechanisms of persistence of Vibrio cholerae . Front Microbiol 2013; 4:375 [View Article]
    [Google Scholar]
  24. Feely RA, Doney SC, Cooley SR. Ocean acidification. Oceanography 2009; 22:36–47
    [Google Scholar]
  25. Byrne RH, Mecking S, Feely RA, Liu X. Direct observations of basin-wide acidification of the North Pacific Ocean. Geophys Res Lett 2010; 37:L02601 [View Article]
    [Google Scholar]
  26. Krause E, Wichels A, Giménez L, Lunau M, Schilhabel MB et al. Small changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS One 2012; 7:e47035 [View Article]
    [Google Scholar]
  27. Thompson JR, Polz MF. Dynamics of Vibrio populations and their role in environmental nutrient cycling. In Thompson FL, Austin B, Swings J. (editors) The Biology of Vibrios Washington, D.C: ASM Press; 2006
    [Google Scholar]
  28. Soto W, Travisano M, Tolleson AR, Nishiguchi MK. Symbiont evolution during the free-living phase can improve host colonization. Microbiology 2019; 165:174–187 [View Article]
    [Google Scholar]
  29. Hughes BS. Evolutionary patterns of Escherichia coli growth in seawater determined with a host to coast environmental laboratory analog. Aquatic Microbial Ecology 2008; 53:243–255 [View Article]
    [Google Scholar]
  30. Hoang KL, Morran LT, Gerardo NM. Experimental evolution as an underutilized tool for studying beneficial animal–microbe interactions. Front Microbiol 2016; 07:1444 [View Article]
    [Google Scholar]
  31. Lenski RE, Rose MR, Simpson SC, Tadler SC. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2000 generations. Am Nat 1991; 138:1315–1341 [View Article]
    [Google Scholar]
  32. McCann J, Stabb EV, Millikan DS, Ruby EG. Population dynamics of Vibrio fischeri during infection of Euprymna scolopes . Appl Environ Microbiol 2003; 69:5928–5934 [View Article]
    [Google Scholar]
  33. Soto W, Rivera FM, Nishiguchi MK. Ecological diversification of Vibrio fischeri serially passaged for 500 generations in novel squid host Euprymna tasmanica . Microb Ecol 2014; 67:700–721 [View Article]
    [Google Scholar]
  34. Ferreira CMH, Pinto ISS, Soares EV, Soares HMVM. (Un)suitability of the use of pH buffers in biological, biochemical and environmental studies and their interaction with metal ions – a review. RSC Adv 2015; 5:30989–31003 [View Article]
    [Google Scholar]
  35. Neidhardt FC, Bloch PL, Smith DF. Culture medium for enterobacteria. J Bacteriol 1974; 119:736–747 [View Article]
    [Google Scholar]
  36. Stoll VS, Blanchard JS. Buffers: principles and practice. Methods Enzymol 1990; 182:24–38 [View Article][PubMed]
    [Google Scholar]
  37. Sokal RR, Rohlf FJ. Biometry, 3rd edn. New York City, New York, United States of America: W.H. Freeman & Company; 1995
    [Google Scholar]
  38. Gerhardt P, Drew SW. Liquid culture. In Gerhardt P, Murray RGE, Wood WA, Krieg NR. (editors) Methods for General and Molecular Bacteriology Washington, DC, United States of America: American Society for Microbiology; 1994
    [Google Scholar]
  39. Hughes BS, Cullum AJ, Bennett AF. Evolutionary adaptation to environmental pH in experimental lineages of Escherichia coli . Evolution 2007; 61:1725–1734 [View Article]
    [Google Scholar]
  40. Hughes BS, Cullum AJ, Bennett AF. An experimental evolutionary study on adaptation to temporally fluctuating pH in Escherichia coli . Physiol Biochem Zool 2007; 80:406–421 [View Article][PubMed]
    [Google Scholar]
  41. Bennett AF, Dao KM, Lenski RE. Rapid evolution in response to high-temperature selection. Nature 1990; 346:79–81 [View Article]
    [Google Scholar]
  42. Zar JH. Biostatistical Analysis, 4th edn. Upper Saddle River, New Jersey, United States of America: Prentice Hall; 1999
    [Google Scholar]
  43. Takahashi T, Sutherland SC, Chipman DW, Goddard JG, Ho C et al. Climatological distributions of pH, pCO2, total CO2, alkalinity, and CaCO3 saturation in the global surface ocean, and temporal changes at selected locations. Mar Chem 2014; 164:95–125 [View Article]
    [Google Scholar]
  44. McFarland WN, Norris KS. The control of pH by buffers in fish transport. California Fish and Game 1958; 44:291–310
    [Google Scholar]
  45. Martin LS, Nieto SR, Sanders BM. Characterization of the cellular stress response in aquatic organisms. In Ostrander GK. editor Techniques in Aquatic Toxicology Volume 1 Boca Raton, Florida, USA: CRC Press; 1996
    [Google Scholar]
  46. McFarland WN, Norris KS. The use of amine buffers in the transportation of fishes. Ann N Y Acad Sci 1961; 92:446–456 [View Article]
    [Google Scholar]
  47. Tyler A, Horowitz NH. Glycylglycine as a sea water buffer. Science 1937; 86:85–86 [View Article]
    [Google Scholar]
  48. Bennett AF, Lenski RE. Evolutionary adaptation to temperature ii. Thermal niches of experimental lines of Escherichia coli . Evolution 1993; 47:1–12 [View Article][PubMed]
    [Google Scholar]
  49. Visick KL, Foster J, Doino J, McFall-Ngai M, Ruby EG. Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 2000; 182:4578–4586 [View Article]
    [Google Scholar]
  50. Kremer N, Schwartzman J, Augustin R, Zhou L, Ruby EG et al. The dual nature of haemocyanin in the establishment and persistence of the squid-Vibrio symbiosis. Proc Biol Sci 2014; 281:20140504 [View Article][PubMed]
    [Google Scholar]
  51. Schwartzman JA, Koch E, Heath-Heckman EAC, Zhou L, Kremer N et al. The chemistry of negotiation: rhythmic, glycan-driven acidification in a symbiotic conversation. Proc Natl Acad Sci U S A 2015; 112:566–571 [View Article]
    [Google Scholar]
  52. Krulwich TA, Sachs G, Padan E. Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 2011; 9:330–343 [View Article]
    [Google Scholar]
  53. Slonczewski JL, Fujisawa M, Dopson M, Krulwich TA. Cytoplasmic pH measurement and homeostasis in bacteria and archaea. Adv Microb Physiol 2009; 55:1–79 [View Article][PubMed]
    [Google Scholar]
  54. Sycuro LK, Ruby EG, McFall-Ngai M. Confocal microscopy of the light organ crypts in juvenile Euprymna scolopes reveals their morphological complexity and dynamic function in symbiosis. J Morphol 2006; 267:555–568 [View Article]
    [Google Scholar]
  55. Milo R, Phillips R. Cell biology by the numbers New York City, New York, United States of America: Garland Science; 2015 p 129
    [Google Scholar]
  56. Wier AM, Nyholm SV, Mandel MJ, Massengo-Tiassé RP, Schaefer AL et al. Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc Natl Acad Sci U S A 2010; 107:2259–2264 [View Article]
    [Google Scholar]
  57. Hansen PJ. Effect of high pH on the growth and survival of marine phytoplankton: implications for species succession. Aquatic Microbial Ecology 2002; 28:279–288 [View Article]
    [Google Scholar]
  58. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S, Ransome E, Fine M et al. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 2008; 454:96–99 [View Article]
    [Google Scholar]
  59. Duarte CM, Hendriks IE, Moore TS, Olsen YS, Steckbauer A et al. Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries and Coasts 2013; 36:221–236 [View Article]
    [Google Scholar]
  60. Soto W, Gutierrez J, Remmenga MD, Nishiguchi MK. Salinity and temperature effects on physiological responses of Vibrio fischeri from diverse ecological niches. Microb Ecol 2009; 57:140–150 [View Article]
    [Google Scholar]
  61. Krissansen-Totton J, Arney GN, Catling DC. Constraining the climate and ocean pH of the early earth with a geological carbon cycle model. Proc Natl Acad Sci U S A 2018; 115:4105–4110 [View Article]
    [Google Scholar]
  62. Gradstein FM, Ogg JG, Smith AG, Bleeker W, Lourens LJ. A new geologic time scale, with special reference to Precambrian and Neogene. Episodes 2004; 27:83–100 [View Article]
    [Google Scholar]
  63. Giggenbach WF. Chemical composition of volcanic gases. In Scarpa R, Tilling R. (editors) Monitoring and Mitigation of Volcano Hazards Berlin, Germany: Springer-Verlag; 1996
    [Google Scholar]
  64. Blättler CL, Kump LR, Fischer WW, Paris G, Kasbohm JJ et al. Constraints on ocean carbonate chemistry and pCO2 in the Archaean and Palaeoproterozoic. Nat Geosci 2017; 10:41–45 [View Article]
    [Google Scholar]
  65. Kempe S, Degens ET. An early soda ocean?. Chem Geol 1985; 53:95–108 [View Article]
    [Google Scholar]
  66. Sleep NH, Zahnle K. Carbon dioxide cycling and implications for climate on ancient earth. J Geophys Res 2001; 106:1373–1399 [View Article]
    [Google Scholar]
  67. Al Rajaibi IM, Hollis C, Macquaker JH. Origin and variability of a terminal Proterozoic primary silica precipitate, Athel Silicilyte, South Oman Salt Basin, Sultanate of Oman. Sedimentology 2015; 62:793–825 [View Article]
    [Google Scholar]
  68. Halevy I, Bachan A. The geologic history of seawater pH. Science 2017; 355:1069–1071 [View Article][PubMed]
    [Google Scholar]
  69. Ridgwell A, Schmidt DN. Past constraints on the vulnerability of marine calcifiers to massive carbon dioxide release. Nat Geosci 2010; 3:196–200 [View Article]
    [Google Scholar]
  70. Blank CE. Phylogenomic dating—a method of constraining the age of microbial taxa that lack a conventional fossil record. Astrobiology 2009; 9:173–191 [View Article]
    [Google Scholar]
  71. Timmins GS, Jackson SK, Swartz HM. The evolution of bioluminescent oxygen consumption as an ancient oxygen detoxification mechanism. J Mol Evol 2001; 52:321–332 [View Article]
    [Google Scholar]
  72. Kuo C-H, Ochman H. Inferring clocks when lacking rocks: the variable rates of molecular evolution in bacteria. Biol Direct 2009; 4:35 [View Article]
    [Google Scholar]
  73. Battistuzzi FU, Feijao A, Hedges SB. A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land. BMC Evol Biol 2004; 4:44 [View Article]
    [Google Scholar]
  74. Hedges S, Blair JE, Venturi ML, Shoe JL. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol Biol 2004; 4:2 [View Article]
    [Google Scholar]
  75. Brocks JJ, Logan GA, Buick R, Summons RE. Archean molecular fossils and the early rise of eukaryotes. Science 1999; 285:1033–1036 [View Article]
    [Google Scholar]
  76. Madigan MT, Bender KS, Buckley DH, Sattley WM, Stahl DA. Brock Biology of Microorganisms New York City, New York, United States of America: Pearson; 2018
    [Google Scholar]
  77. Müller M, Martin W. The genome of Rickettsia prowazekii and some thoughts on the origin of mitochondria and hydrogenosomes. Bioessays 1999; 21:377–381 [View Article][PubMed]
    [Google Scholar]
  78. Margulis L. Symbiosis in Cell Evolution, 2nd edn. San Francisco, California, United States of America: W.H. Freeman; 1992
    [Google Scholar]
  79. Abd H, Saeed A, Weintraub A, Nair GB, Sandström G. Vibrio cholerae O1 strains are facultative intracellular bacteria, able to survive and multiply symbiotically inside the aquatic free-living amoeba Acanthamoeba castellanii . FEMS Microbiol Ecol 2007; 60:33–39 [View Article]
    [Google Scholar]
  80. Dobretsov S. Marine biofilms. In Dürr S, Thomason JC. (editors) Biofouling Chichester, Great Britain: Wiley-Blackwell; 2010
    [Google Scholar]
  81. Tivey M. Generation of seafloor hydrothermal vent fluids and associated mineral deposits. Oceanography 2007; 20:50–65 [View Article]
    [Google Scholar]
  82. Hasan NA, Grim CJ, Lipp EK, Rivera ING, Chun J et al. Deep-sea hydrothermal vent bacteria related to human pathogenic Vibrio species. Proc Natl Acad Sci U S A 2015; 112:E2813–E2819 [View Article]
    [Google Scholar]
  83. Raguénès G, Christen R, Guezennec J, Pignet P, Barbier G et al. Vibrio diabolicus sp. nov., a new polysaccharide-secreting organism isolated from a deep-sea hydrothermal vent polychaete annelid, Alvinella pompejana . International Journal of Systematic and Evolutionary Microbiology 1997; 47:989–995
    [Google Scholar]
  84. Steenackers HP, Parijs I, Foster KR, Vanderleyden J. Experimental evolution in biofilm populations. FEMS Microbiol Rev 2016; 40:373–397 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000884
Loading
/content/journal/micro/10.1099/mic.0.000884
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error