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Ecological Adaptability of Bacillus to Extreme Oligotrophy in the Cuatro Cienegas Basin

  • Jorge Valdivia-Anistro
  • Luis E. Eguiarte
  • Valeria Souza
Chapter
Part of the Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis book series (CUCIBA)

Abstract

The genus Bacillus is known for its ability to colonize diverse environments and to take up a wide variety of resources. Both properties are linked to its spore-forming life history strategy and to its high number of rrn operon copies per genome. Experimental evidence has postulated a relationship between the number of copies of the rrn operon and the availability of environmental phosphorus. Generally, aquatic bacteria isolated from oligotrophic environments have few rrn operon copies and other adaptations that decrease cellular phosphorus demand. The Cuatro Cienegas Basin (CCB) is an aquatic ecosystem with extreme oligotrophy and with high diversity of Bacillus strains. For this reason, we explored the variation of the rrn operon copy number in different Bacillus lineages and their physiological implications during growth under oligotrophic conditions. Unexpectedly, the Bacillus from the CCB has a high variation in the number of rrn operon copies despite the extreme phosphorus limitation in this environment. In addition, these bacilli showed different ecological responses reflected in the heterogeneity of their growth dynamics. This heterogeneity seems to be a response to the low availability of nutrients and the competitive cost represented by a high number of rrn operon copies. Interestingly, the cellular stoichiometry and protein content during growth dynamics of these Bacillus are not consistent with the growth rate hypothesis. The ecological adaptability of the genus Bacillus to the oligotrophy of the CCB appears to be due to its high heterogeneity in the number of copies of the rrn operon, its cellular stoichiometry, and its ecophysiological adaptations.

Keywords

Aquatic bacteria Bacillus Growth Rate Hypothesis Phosphorus rrn operon 

References

  1. Acinas SG, Marcelino LA, Klepac-Ceraj V et al (2004) Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 186:2629–2635CrossRefGoogle Scholar
  2. Alcaraz LD, Olmedo G, Bonilla G et al (2008) The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment. PNAS 105:5803–5808. https://doi.org/10.1073/pnas.0800981105 CrossRefPubMedGoogle Scholar
  3. Alcaraz LD, Moreno-Hagelsieb G, Eguiarte LE et al (2010) Understanding the evolutionary relationships and major traits of Bacillus through comparative genomics. BMC Genomics 11:332. https://doi.org/10.1186/1471-2164-11-332 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Antolinos V, Muñoz M, Ros-Chumillas M et al (2011) Combined effect of lysozyme and nisin at different incubation temperature and mild heat treatment on the probability of time growth of Bacillus cereus. Food Microbiol 28:305–310. https://doi.org/10.1016/j.fm.2010.07.021 CrossRefPubMedGoogle Scholar
  5. Antolinos V, Muñoz-Cuevas M, Ros-Chumillas M et al (2012) Modelling the effects of temperature and osmotic shifts on the growth kinetics of Bacillus weihenstephanensis in broth and food products. Int J Food Microbiol 158:36–41. https://doi.org/10.1016/j.ijfoodmicro.2012.06.017 CrossRefPubMedGoogle Scholar
  6. Carini P, Van Mooy BA, Thrash JC et al (2015) SAR11 lipid renovation in response to phosphate starvation. PNAS 112:7767–7772. https://doi.org/10.1073/pnas.1505034112 CrossRefPubMedGoogle Scholar
  7. Cerritos R, Vinuesa P, Eguiarte LE et al (2008) Bacillus coahuilensis sp. nov., a moderately halophilic species from a desiccated lagoon in the Cuatro Cienegas valley in Coahuila, Mexico. Int J Syst Evol Microbiol 58:919–923. https://doi.org/10.1099/ijs.0.64959-0 CrossRefPubMedGoogle Scholar
  8. Cescutti G, Matteucci F, Caffau E et al (2012) Chemical evolution of the Milky Way: the origin of phosphorus. Astron Astrophys 540. https://doi.org/10.1051/0004-6361/201118188 CrossRefGoogle Scholar
  9. Chubukov V, Sauer U (2014) Environmental dependence of stationary-phase metabolism in Bacillus subtilis and Escherichia coli. Appl Environ Microbiol 80:2901–2909. https://doi.org/10.1128/AEM.00061-14 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Codon C, Liveris D, Squires C et al (1995) rRNA operon multiplicity in Escherichia coli and the physiological implications of rrn inactivation. J Bacteriol 177:4152–4156CrossRefGoogle Scholar
  11. Des Marais DJ, Walter MR (1999) Astrobiology: exploring the origins, evolution, and distribution of life in the universe. Annu Rev Ecol Syst 30:397–420CrossRefGoogle Scholar
  12. Dethlefsen L, Schmidt TM (2007) Performance of the translational apparatus varies with the ecological strategies of bacteria. J Bacteriol 189:3237–3245CrossRefGoogle Scholar
  13. Elser JJ (2003) Biological stoichiometry: a theoretical framework connecting ecosystem ecology, evolution, and biochemistry for application in astrobiology. Int J Astrobiology 2, 185–193. https://doi.org/10.1017/S1473550403001563 CrossRefGoogle Scholar
  14. Elser JJ (2006) Biological stoichiometry: a chemical bridge between ecosystem ecology and evolutionary biology. Am Nat 168(Suppl. 6):S25–S35CrossRefGoogle Scholar
  15. Elser JJ, Hamilton A (2007) Stoichiometry and the New Biology: the future is now. PLoS Biol 5(7):e181. https://doi.org/10.1371/journal.pbio.0050181 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Elser JJ, Sterner RW, Gorokhova E et al (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550CrossRefGoogle Scholar
  17. Emir R, Yusof N, Patermann I et al (2013) On the nucleosynthesis of phosphorus in massive stars. AIP Conf Proc 1528:62. https://doi.org/10.1063/1.4803569 CrossRefGoogle Scholar
  18. Fegatella F, Lim J, Kjelleberg S et al (1998) Implications of rRNA operon copy number and ribosome content in the marine oligotrophic ultramicrobacterium Sphingomonas sp. strain RB2256. Appl Environ Microbiol 64:4433–4438PubMedPubMedCentralGoogle Scholar
  19. Feldgarden M, Byrd N, Cohan FM (2003) Gradual evolution in bacteria: evidence from Bacillus systematics. Microbiology 149:3565–3573CrossRefGoogle Scholar
  20. Goelzer A, Fromion V (2011) Bacterial growth rate reflects a bottleneck in resource allocation. Biochim Biophys Acta 1810:978–988. https://doi.org/10.1016/j.bbagen.2011.05.014 CrossRefPubMedGoogle Scholar
  21. Green JL, Bohannan BJM, Whitaker RJ (2008) Microbial biogeography: from taxonomy to traits. Science 320:039–1042. https://doi.org/10.1126/science.1153475 CrossRefGoogle Scholar
  22. Jeyasingh PD, Weider LJ (2007) Fundamental links between genes and elements: evolutionary implications of ecological stoichiometry. Mol Ecol 16:4649–4661. https://doi.org/10.1111/j.1365-294X.2007.03558.x CrossRefPubMedGoogle Scholar
  23. Jones RD (2002) Phosphorus cycling. In: Hurst CJ, Crawford RL, Knudsen GR et al (eds) Manual of environmental microbiology. ASM Press, Washington, DC, pp 450–455Google Scholar
  24. Klappenbach JA, Dunbar JM, Schmidt TM (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66:1328–1333CrossRefGoogle Scholar
  25. Klumpp S, Zhang Z, Hwa T (2009) Growth rate-dependent global effects on gene expression in bacteria. Cell 139:1366–1375. https://doi.org/10.1016/j.cell.2009.12.001 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lauro FM, McDougald D, Thomas T et al (2009) The genomic basis of trophic strategy in marine bacteria. PNAS 106:5527–15533. https://doi.org/10.1073/pnas.0903507106 CrossRefGoogle Scholar
  27. Loladze I, Elser JJ (2011) The origins of the Redfield nitrogen-to-phosphorus ratio are in a homoeostatic protein-to-rRNA ratio. Ecol Lett 14:244–250. https://doi.org/10.1111/j.1461-0248.2010.01577.x CrossRefPubMedGoogle Scholar
  28. Luo H, Friedman R, Tang J et al (2011) Genome reduction by deletions of paralogs in the marine cyanobacterium Prochlorococcus. Mol Biol Evol 28:2751–2760. https://doi.org/10.1093/molbev/msr081 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Maciá E (2005) The role of phosphorus in chemical evolution. Chem Soc Rev 34:691–701CrossRefGoogle Scholar
  30. Martiny AC, Coleman ML, Chisholm SW (2006) Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. PNAS 103:12552–12557CrossRefGoogle Scholar
  31. Martiny AC, Huang Y, Li W (2009) Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions. Environ Microbiol 11:1340–1347. https://doi.org/10.1111/j.1462-2920.2009.01860.x CrossRefPubMedGoogle Scholar
  32. Moreno-Letelier A, Olemdo G, Eguiarte LE et al (2011) Parallel evolution and horizontal gene transfer of the pst operon in Firmicutes from oligotrophic environments. Int J Evol Biol 2011:781642. https://doi.org/10.4061/2011/781642 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Neidhardt FC (1999) Bacterial growth: constant obsession with dN/dt. J Bacteriol 181:7405–7408PubMedPubMedCentralGoogle Scholar
  34. Oren A (2004) Prokaryote diversity and taxonomy: current status and future challenges. Philos Trans R Soc B Biol Sci 359:623–638CrossRefGoogle Scholar
  35. Pasek MA (2008) Rethinking early Earth phosphorus geochemistry. PNAS 105:853–858. https://doi.org/10.1073/pnas.0708205105 CrossRefPubMedGoogle Scholar
  36. Pasek MA, Herschy B, Kee TP (2015) Phosphorus: a case for mineral-organic reactions in prebiotic chemistry. Orig Life Evol Biosph 45:207–218. https://doi.org/10.1007/s11084-015-9420-y CrossRefPubMedGoogle Scholar
  37. Paytan A, McLaughlin K (2007) The oceanic phosphorus cycle. Chem Rev 107:563–576CrossRefGoogle Scholar
  38. Rastogi R, Wu M, Dasgupta I et al (2009) Visualization of ribosomal RNA operon copy number distribution. BMC Microbiol 9:208. https://doi.org/10.1186/1471-2180-9-208 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Schaechter M (2006) From growth physiology to system biology. Int Microbiol 9:157–161PubMedGoogle Scholar
  40. Schwartz AW (2006) Phosphorus in prebiotic chemistry. Philos Trans R Soc Lond B Biol Sci 361:1743–1749; discussion 1749CrossRefGoogle Scholar
  41. Scott M, Hwa T (2011) Bacterial growth laws and their applications. Curr Opin Biotechnol 22:559–565. https://doi.org/10.1016/j.copbio.2011.04.014 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Scott M, Gunderson CW, Mateescu EM et al (2010) Interdependence of cell growth and gene expression: origins and consequences. Science 330:1099–1102. https://doi.org/10.1126/science.1192588 CrossRefPubMedGoogle Scholar
  43. Sebastián M, Smith AF, González JM et al (2016) Lipid remodelling is a widespread strategy in marine heterotrophic bacteria upon phosphorus deficiency. ISME J 10:968–978. https://doi.org/10.1038/ismej.2015.172 CrossRefPubMedGoogle Scholar
  44. Shrestha PM, Noll M, Liesack W (2007) Phylogenetic identity, growth-response time and rRNA operon copy number of soil bacteria indicate different stages of community succession. Enviro Microbiol 9:2464–2474CrossRefGoogle Scholar
  45. Souza V, Eguiarte LE, Siefert JS et al (2008) Microbial endemism: does phosphorus limitation enhance speciation? Nat Rev Microbiol 6:559–564. https://doi.org/10.1038/nrmicro1917 CrossRefPubMedGoogle Scholar
  46. Souza V, Siefert JL, Escalante AE et al (2012) The Cuatro Ciénegas Basin in Coahuila, Mexico: an astrobiological Precambrian park. Astrobiology 12:641–647. https://doi.org/10.1089/ast.2011.0675 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Stevenson BS, Schmidt TM (2004) Life history implications of rRNA gene copy number in Escherichia coli. Appl Environ Microbiol 70:6670–6677CrossRefGoogle Scholar
  48. Stoddard SF, Smith BJ, Hein R et al (2015) rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res 43:D593–D598. https://doi.org/10.1093/nar/gku1201 CrossRefPubMedGoogle Scholar
  49. Strehl B, Holtzendorff J, Partensky F et al (1999) A small and compact genome in the marine cyanobacterium Prochlorococcus marinus CCMP 1375: lack of an intron in the gene for tRNAr (Leu)UAA and a single copy of the rRNAop. FEMS Microbiol Lett 181:261–266CrossRefGoogle Scholar
  50. Sun Z, Blanchard JL (2014) Strong genome-wide selection early in the evolution of Prochlorococcus resulted in a reduced genome through the loss of a large number of small effect genes. PLoS One 9(3):e88837. https://doi.org/10.1371/journal.pone.0088837 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Valdivia-Anistro JA, Eguiarte-Fruns LE, Delgado-Sapién G et al (2016) Variability of rRNA operon copy number and growth rate dynamics of Bacillus isolated from an extremely oligotrophic aquatic ecosystem. Front Microbiol 6:1486. https://doi.org/10.3389/fmicb.2015.01486 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Valík L, Görner F, Lauková D (2003) Growth dynamics of Bacillus cereus and self-life of pasteurised milk. Czech J Food Sci 21:195–202CrossRefGoogle Scholar
  53. Vishnivetskaya TA, Kathariou S, Tiedje JM (2009) The Exiguobacterium genus: biodiversity and biogeography. Extremophiles 13:541–555. https://doi.org/10.1007/s00792-009-0243-5 CrossRefPubMedGoogle Scholar
  54. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. PNAS 95:6578–6583CrossRefGoogle Scholar
  55. Yano K, Wada T, Suzuki S et al (2013) Multiple rRNA operons are essential for efficient cell growth and sporulation as well as outgrowth in Bacillus subtilis. Microbiology 159:2225–2236. https://doi.org/10.1099/mic.0.067025-0 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Jorge Valdivia-Anistro
    • 1
  • Luis E. Eguiarte
    • 2
  • Valeria Souza
    • 2
  1. 1.Facultad de Estudios Superiores ZaragozaUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMéxico
  2. 2.Departamento de Ecología EvolutivaInstituto de Ecología, Universidad Nacional Autónoma de MéxicoCiudad de MéxicoMéxico

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