How Divergent Is the Cuatro Ciénegas Oasis? Genomic Studies of Microbial Populations and Niche Differentiation

  • Zulema Gomez-Lunar
  • Mirna Vázquez-Rosas-Landa
  • Gabriel Yaxal Ponce-Soto
  • Alejandra Moreno-Letelier
  • Gabriela Olmedo-Álvarez
  • Luis E. Eguiarte
  • Valeria Souza
Part of the Cuatro Ciénegas Basin: An Endangered Hyperdiverse Oasis book series (CUCIBA)


In this chapter, we describe some genomic studies that have been conducted in the CCB to describe the microdiversity of different microbial taxa. Firstly, we describe the genomic variation in the endemic species B. coahuilensis, for which we analyzed three strains, and the evolutionary mechanism that have shaped their genomes, in particular for their adaptations to a low phosphorus environment. Secondly, we describe population genomics of Proteobacteria such as Pseudomonas, Vibrio, Photobacterium, and Aeromonas, finding many genes related to bacterial interactions, such as type III and VI secretion systems, which led us to propose that these systems play an important role in interactions among bacterial communities. Many of these interaction genes have been classified previously as virulence factors. However, at CCB these genes were not found in a cassette configuration—such as an integron or a pathogenicity island—in any strain suggesting that they are very ancestral adaptive responses to keep both the cohesion within the community and the cheaters out of the community. Interestingly, even if B. coahuilensis presents many mobile elements, these elements are rare in the surveyed Proteobacteria, whose genomes present many CRISPS elements. The presence of CRISPR regions may also explain why there are few ISs or plasmids since it has been reported that CRISPR spacers can act as barriers against HGT.



The research was funded in part by Papiit-UNAM project IG200215 for Vibrio comparative genomics to VS and LEE, and CONACYT CB-2013-01 No. 220536 to GO-A. This chapter was written during a sabbatical leave of VS in the Department of Ecology, Evolution, and Behavior, University of Minnesota in Dr. Michael Travisano´s laboratory, and of LEE, in the Department of Plant and Microbial Biology, University of Minnesota in Dr. Peter Tiffin’s laboratory, both supported by the program PASPA-DGAPA, UNAM.


  1. Abby S, Daubin V (2007) Comparative genomics and the evolution of prokaryotes. Trends Microbiol 15(3):135–141CrossRefGoogle Scholar
  2. Alcaraz LD et al (2008) The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment. Proc Natl Acad Sci 105(15):5803–5808CrossRefGoogle Scholar
  3. Ali M, Nelson AR, Lopez AL, Sack D (2015) Updated global burden of cholera in endemic countries. PLoS Negl Trop Dis 9(6):e0003832CrossRefGoogle Scholar
  4. Allenby NEE et al (2005) Genome-wide transcriptional analysis of the phosphate starvation stimulon of Bacillus subtilis. J Bacteriol 187(23):8063–8080CrossRefGoogle Scholar
  5. Antelmann H, Scharf C, Hecker M (2000) Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J Bacteriol 182(16):4478–4490CrossRefGoogle Scholar
  6. Arocha-Garza HF et al (2017) High diversity and suggested endemicity of culturable Actinobacteria in an extremely oligotrophic desert oasis. PeerJ 5:e3247CrossRefGoogle Scholar
  7. Bland C et al. (2007) CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinformatics 8(1):209(1–19) CrossRefGoogle Scholar
  8. Breitbart M et al (2009) Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Ciénegas, Mexico. Environ Microbiol 11(1):16–34CrossRefGoogle Scholar
  9. Brown M, Fuhrman J (2005) Marine bacterial microdiversity as revealed by internal transcribed spacer analysis. Aquat Microb Ecol 41(1):15–23CrossRefGoogle Scholar
  10. Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann ML, Brussow H (2003) Phage as agents of lateral gene transfer. Curr Opin Microbiol 6(4):417–424CrossRefGoogle Scholar
  11. Cerritos R et al (2011) Diversity of culturable thermo-resistant aquatic bacteria along an environmental gradient in Cuatro Cienegas, Coahuila, Mexico. Antonie Van Leeuwenhoek 99(2):303–318CrossRefGoogle Scholar
  12. Choi M, Stevens AM, Smith SA, Taylor DP, Kuhn DD (2017) Strain and dose infectivity of Vibrio parahaemolyticus: the causative agent of early mortality syndrome in shrimp. Aquac Res 48:3719–3727CrossRefGoogle Scholar
  13. Chong H, Li Q (2017) Microbial production of rhamnolipids: opportunities, challenges and strategies. Microb Cell Factories 16:137CrossRefGoogle Scholar
  14. Choudhary DK, Johri BN (2011) Ecological significance of microdiversity: coexistence among casing soil bacterial strains through allocation of nutritional resource. Indian J Microbiol 51(1):8–13CrossRefGoogle Scholar
  15. Colwell RR, MacDonell MT, DeLey J (1986) Proposal to recognize the family Aeromonadaceae fam. nov. Int J Syst Bacteriol 36:473–477CrossRefGoogle Scholar
  16. Cristobal-Azkarate J, Dunn JC, Day JMW, Amabile-Cuevas CF (2014) Resistance to antibiotics of clinical relevance in the fecal microbiota of Mexican wildlife. PLoS ONE 9(9):e107719. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cury J et al. (2016) Identification and analysis of integrons and cassette arrays in bacterial genomes. Nucleic Acids Research 4(10):4539–4550.CrossRefGoogle Scholar
  18. de Souza JT, De Boer M, De Waard P, Van Beek TA, Raaijmakers JM (2003) Biochemical, genetic, and zoosporicidal properties of cyclic lipopeptide surfactants produced by Pseudomonas fluorescens. Appl Environ Microbiol 69:7161–7172CrossRefGoogle Scholar
  19. Deng X et al (2010) Probing the pan-genome of Listeria monocytogenes: new insights into intraspecific niche expansion and genomic diversification. BMC Genomics 11:500CrossRefGoogle Scholar
  20. Dobrindt U, Hochhut B, Hentschel U, Hacker J (2004) Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2(5):414–424. CrossRefPubMedGoogle Scholar
  21. Escalante AE et al (2008) Diversity of aquatic prokaryotic communities in the Cuatro Cienegas basin. FEMS Microbiol Ecol 65(1):50–60CrossRefGoogle Scholar
  22. Escalante AE et al (2009) Pseudomonas cuatrocienegasensis sp. nov., isolated from an evaporating lagoon in the Cuatro Cienegas valley in Coahuila, Mexico. International Journal of Systematic and Evolutionary Microbiology 59(6):1416–1420.CrossRefGoogle Scholar
  23. Fuhrman JA, Campbell L (1998) Microbial microdiversity. Nature 393(6684):410–411CrossRefGoogle Scholar
  24. García-Martinez J, Rodriguez-Valera F (2000) Microdiversity of uncultured marine prokaryotes: the SAR11 cluster and the marine Archaea of Group I. Mol Ecol 9(7):935–948CrossRefGoogle Scholar
  25. García-Gutiérrez E et al. (2015) CRISPR Content Correlates with the Pathogenic Potential of Escherichia coli. PLoS ONE 10(7):e0131935. CrossRefGoogle Scholar
  26. Giovannoni SJ et al (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309(5738):1242–1245CrossRefGoogle Scholar
  27. Gómez-Lunar Z et al (2016) Microevolution analysis of Bacillus coahuilensis unveils differences in phosphorus acquisition strategies and their regulation. Front Microbiol 7:58CrossRefGoogle Scholar
  28. Hazen TH, Pan L, Gu JD, Sobecky PA (2010) The contribution of mobile genetic elements to the evolution and ecology of Vibrios. FEMS Microbiol Ecol 74(3):485–499. CrossRefPubMedGoogle Scholar
  29. Henkel M, Geissler M, Weggenmann F, Hausmann R (2017) Production of microbial biosurfactants: status quo of rhamnolipid and surfactin towards large-scale production. Biotechnol J 12(7):28544628. CrossRefGoogle Scholar
  30. Hernández-González IL, Olmedo-Álvarez G (2016a) Draft whole-genome sequence of the type strain Bacillus horikoshii DSM 8719. Genome Announc 4(4):e00640–e00616PubMedPubMedCentralGoogle Scholar
  31. Hernández-González IL, Olmedo-Álvarez G (2016b) Draft whole-genome sequence of the type strain Bacillus aquimaris TF12 T. Genome Announc 4(4):e00641–e00616PubMedPubMedCentralGoogle Scholar
  32. Jaspers E, Overmann J (2004) Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl Environ Microbiol 70(8):4831–4839CrossRefGoogle Scholar
  33. Jiang SC, Paul JH (1998) Gene transfer by transduction in the marine environment. Appl Environ Microbiol 64(8):2780–2787PubMedPubMedCentralGoogle Scholar
  34. Jonas S et al (2008) A new member of the alkaline phosphatase superfamily with a formylglycine nucleophile: structural and kinetic characterisation of a phosphonate monoester hydrolase/phosphodiesterase from Rhizobium leguminosarum. J Mol Biol 384(1):120–136CrossRefGoogle Scholar
  35. Kalhoefer D et al (2011) Comparative genome analysis and genome-guided physiological analysis of Roseobacter litoralis. BMC Genomics 12:324CrossRefGoogle Scholar
  36. Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Philos Trans R Soc B 361(1475):1929–1940CrossRefGoogle Scholar
  37. Koonin EV, Wolf YI (2008) Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36(21):6688–6719CrossRefGoogle Scholar
  38. Kulakovskaya T (2014) Phosphorus storage in microorganisms: diversity and evolutionary insight. Biochem Physiol 4(1):e130CrossRefGoogle Scholar
  39. Larkin AA, Martiny AC (2017) Microdiversity shapes the traits, niche space, and biogeography of microbial taxa. Environ Microbiol Rep 9(2):55–70CrossRefGoogle Scholar
  40. Luo H, Moran MA (2015) How do divergent ecological strategies emerge among marine bacterioplankton lineages? Trends Microbiol 23(9):577–584CrossRefGoogle Scholar
  41. Mann RA et al (2013) Comparative genomics of 12 strains of Erwinia amylovora identifies a pan-genome with a large conserved core. PLoS One 8(2):e55644CrossRefGoogle Scholar
  42. Martin P et al (2014) Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus. Proc Natl Acad Sci 111(22):8089–8094CrossRefGoogle Scholar
  43. Math RK et al (2012) Comparative genomics reveals adaptation by Alteromonas sp. SN2 to marine tidal-flat conditions: cold tolerance and aromatic hydrocarbon metabolism. PLoS One 7(4):e35784CrossRefGoogle Scholar
  44. Mazel D, Dychinco B, Webb VA, Davies J (1998) A distinctive class of integron in the Vibrio cholerae genome. Science 280(5363):605–608CrossRefGoogle Scholar
  45. Meyer JL, Huber JA (2014) Strain-level genomic variation in natural populations of Lebetimonas from an erupting deep-sea volcano. Int Soc Microb Ecol J 8(4):867–880Google Scholar
  46. Mira A, Klasson L, Andersson SGE (2002) Microbial genome evolution: sources of variability. Curr Opin Microbiol 5(5):506–512CrossRefGoogle Scholar
  47. Mira A, Ochman H, Moran NA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17(10):589–596CrossRefGoogle Scholar
  48. Moon BY, Park JY, Robinson DA, Thomas JC, Park YH, Thornton JA, Seo KS (2016) Mobilization of genomic islands of Staphylococcus aureus by temperate bacteriophage. PLoS ONE 11(3):e0151409. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Moore LR, Rocap G, Chisholm SW (1998) Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393(6684):464–467CrossRefGoogle Scholar
  50. Morris JJ, Lenski RE, Zinser ER (2012) The black queen hypothesis: evolution of dependencies through adaptive gene loss. MBio 3(2):e00036-12CrossRefGoogle Scholar
  51. Ochman H, Davalos LM (2006) The nature and dynamics of bacterial genomes. Science 311(5768):1730–1733CrossRefGoogle Scholar
  52. Patiño-Navarrete R et al (2013) Comparative genomics of Blattabacterium cuenoti: the frozen legacy of an ancient endosymbiont genome. Genome Biol Evol 5(2):351–361CrossRefGoogle Scholar
  53. Peña A et al (2010) Fine-scale evolution: genomic, phenotypic and ecological differentiation in two coexisting Salinibacter ruber strains. Int Soc Microb Ecol J 4(7):882–895Google Scholar
  54. Penn K, Jensen PR (2012) Comparative genomics reveals evidence of marine adaptation in Salinispora species. BMC Genomics 13:86CrossRefGoogle Scholar
  55. Ponce-Soto GY, Aguirre-von-Wobeser E, Eguiarte LE, Elser JJ, Lee ZMP, Souza V (2015) Enrichment experiment changes microbial interactions in an ultra-oligotrophic environment. Front in Microbiology 6(246).
  56. Quinn JP et al (2007) New ways to break an old bond: the bacterial carbon-phosphorus hydrolases and their role in biogeochemical phosphorus cycling. Environ Microbiol 9(10):2392–2400CrossRefGoogle Scholar
  57. Rodríguez-Verdugo A, Souza V, Eguiarte LE, Escalante AE (2012) Diversity across seasons of culturable Pseudomonas from a desiccation lagoon in Cuatro Cienegas, Mexico. International Journal of Microbiology 212: 10. CrossRefGoogle Scholar
  58. Schloter M et al (2000) Ecology and evolution of bacterial microdiversity. FEMS Microbiol Rev 24(5):647–660CrossRefGoogle Scholar
  59. Sheludchenko MS, Huygens F, Stratton H, Hargreaves M (2015) CRISPR Diversity in E. coli Isolates from Australian Animals, Humans and Environmental Waters. PLoS ONE 10(5):e0124090. CrossRefGoogle Scholar
  60. Singh DN et al (2015) Identification and characterization of a novel phosphodiesterase from the metagenome of an Indian coalbed. PLoS One 10(2):e0118075CrossRefGoogle Scholar
  61. Soberón J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett, 10:1115–1123CrossRefGoogle Scholar
  62. Souza V et al (2006) An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert. Proc Natl Acad Sci 103(17):6565–6570CrossRefGoogle Scholar
  63. Souza V, Siefert JL, Escalante AE, Elser JJ, Eguiarte LE (2012). The Cuatro Ciénegas Basin in Coahuila, Mexico: An Astrobiological Precambrian Park. Astrobiology, 12(7):641–647. CrossRefGoogle Scholar
  64. Stover CK et al (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406(6799):959CrossRefGoogle Scholar
  65. Tian CF et al (2012) Comparative genomics of rhizobia nodulating soybean suggests extensive recruitment of lineage-specific genes in adaptations. Proc Natl Acad Sci 109(22):8629–8634CrossRefGoogle Scholar
  66. Vázquez-Rosas-Landa M, Yaxal Ponce-Soto G, Eguiarte LE, Souza V (2017) Comparative genomics of free-living Gammaproteobacteria: pathogenesis-related genes or interaction-related genes?. FEMS Pathogens and Disease 75(5):1–12Google Scholar
  67. Vélez P, Gasca-Pineda J, Rosique-Gil E, Eguiarte LE, Espinosa-Asuar L, Souza V (2016) Microfungal oasis in an oligotrophic desert: diversity patterns and community structure in three freshwater systems of Cuatro Ciénegas, Mexico. PeerJ, 4, e2064. CrossRefGoogle Scholar
  68. Vershinina OA, Znamenskaya LV (2002) The pho regulons of bacteria. Microbiology 71(5):497–511CrossRefGoogle Scholar
  69. Villarreal-Chiu JF, Quinn JP, McGrath JW (2012) The genes and enzymes of phosphonate metabolism by bacteria, and their distribution in the marine environment. Front Microbiol 3:1–13CrossRefGoogle Scholar
  70. Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6(1):1–11CrossRefGoogle Scholar
  71. Weitz JS, Wilhelm SW (2012) Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biol Rep 4:17. CrossRefPubMedPubMedCentralGoogle Scholar
  72. Yoshida S, Ohba A, Liang YM, Koitabashi M, Tsushima S (2012) Specificity of Pseudomonas isolates on healthy and Fusarium head blight-infected spikelets of wheat heads. Microb Ecol 64(1):214–225. CrossRefPubMedGoogle Scholar
  73. Zarza E, Alcaraz LD, Aguilar-Salinas B, Islas A, Olmedo-Álvarez A (2017) Complete genome sequence of Bacillus horikoshii strain 20a from Cuatro Cienegas, Coahuila, Mexico. Genome Announc 5(30):e00592-17CrossRefGoogle Scholar
  74. Zimmerman AE, Martiny AC, Allison SD (2013) Microdiversity of extracellular enzyme genes among sequenced prokaryotic genomes. ISME J 7(6):1187–1199CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Zulema Gomez-Lunar
    • 1
  • Mirna Vázquez-Rosas-Landa
    • 2
  • Gabriel Yaxal Ponce-Soto
    • 2
  • Alejandra Moreno-Letelier
    • 3
  • Gabriela Olmedo-Álvarez
    • 1
  • Luis E. Eguiarte
    • 2
  • Valeria Souza
    • 2
  1. 1.Laboratorio de Biología Molecular y Ecología Microbiana, Departamento de Ingeniería GenéticaUnidad Irapuato, Centro de Investigación y de Estudios Avanzados del IPNIrapuatoMexico
  2. 2.Laboratorio de Evolución Molecular y Experimental, Departamento de Ecología Evolutiva, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMexico CityMexico
  3. 3.Jardín BotánicoInstituto de Biología Universidad Nacional Autónoma de MéxicoMexico CityMexico

Personalised recommendations