Skip to main content

Advertisement

SpringerLink
Log in

Bacterial Diversity in the Soda Saline Crater Lake from Isabel Island, Mexico

  • Environmental Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Isabel Lake is a moderate saline soda crater lake located in Isabel Island in the eastern tropical Pacific coast of Mexico. Lake is mainly formed by rainfall and is strongly affected by evaporation and high input of nutrients derived from excretions of a large bird community inhabiting the island. So far, only the island macrobiota has been studied. The knowledge of the prokaryotic biota inhabiting the upper layers of this meromictic lake can give clues for the maintenance of this ecosystem. We assessed the diversity and composition of prokaryotic community in sediments and water of the lake by DGGE profiling, 16S rRNA gene amplicon pyrosequencing, and cultivation techniques. The bacterial community is largely dominated by halophilic and halotolerant microorganisms. Alpha diversity estimations reveal higher value in sediments than in water (P > 0.005). The lake water is dominated by γ-Proteobacteria belonging to four main families where Halomonadaceae presents the highest abundance. Aerobic, phototrophic, and halotolerant prokaryotes such as Cyanobacteria GPIIa, Halomonas, Alcanivorax, Idiomarina, and Cyclobacterium genera are commonly found. However, in sediment samples, Formosa, Muricauda, and Salegentibacter genera corresponding to Flavobacteriaceae family accounted for 15–20 % of the diversity. Heterotrophs like those involved in sulfur cycle, Desulfotignum, Desulfuromonas, Desulfofustis, and Desulfopila, appear to play an important role in sediments. Finally, a collection of aerobic halophilic bacterial isolates was created from these samples; members of the genus Halomonas were predominantly isolated from lake water. This study contributes to state the bacterial diversity present in this particular soda saline crater lake.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Ortega GF, González GR (1980) Nódulos de peridotita en la isla Isabel, Nayarit. Universidad Nacional Autónoma de México. Rev Mex Cienc Geol 4:82–83

    Google Scholar 

  2. Sorokin DY, Berben T, Melton ED, Overmars L, Vavourakis CD, Muyzer G (2014) Microbial diversity and biogeochemical cycling in soda lakes. Extremophiles 18:791–809

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  3. Hahn IJ, Hogeback S, Romer U, Vergara PM (2012) Biodiversity and biogeography of birds in Pacific Mexico along an isolation gradient from mainland Chamela via coastal Marias to oceanic Revillagigedo Islands. Vertebr Zool 62:123–144

    Google Scholar 

  4. Alcocer J, Lugo A, Sánchez MR, Escobar E (1998) Isabela Crater-Lake: a Mexican insular saline lake. Hydrobiologia 381:1–7

    Article  CAS  Google Scholar 

  5. Diario Oficial de la Federación (1980). Decreto por el que se declara Parque Nacional a la Isla Isabel, ubicada frente a las costas del Estado de Nayarit, declarándose de interés público la conservación y aprovechamiento de sus valores naturales, para fines recreativos, culturales y de investigación científica. http://dof.gob.mx/nota_detalle.php?codigo=4862220&fecha=08/12/1980

  6. Grant WD (1992) Alkaline environments. In: Lederberg journal of encyclopedia of microbiology. Academic Press, London 1: 73–80

  7. Mesbah NM, Abou-El-Ela SH, Wiegel J (2007) Novel and unexpected prokaryotic diversity in water and sediments of the alkaline, hypersaline lakes of the Wadi An Natrun, Egypt. Microb Ecol 54:598–617

    Article  PubMed  CAS  Google Scholar 

  8. Hollister EB, Engledow AS, Hammett AJ, Provin TL, Wilkinson HH, Gentry TJ (2010) Shifts in microbial community structure along an ecological gradient of hypersaline soils and sediments. ISME J 4:829–838

    Article  PubMed  CAS  Google Scholar 

  9. Tourova TP, Slobodova NV, Bumazhkin BK, Kolganova TV, Muyzer G, Dimitry Sorokin DY (2012) Analysis of community composition of sulfur-oxidizing bacteria in hypersaline and soda lakes using soxB as a functional molecular marker. FEMS Microbiol Ecol 84:280–289

    Article  PubMed  Google Scholar 

  10. Zavarzin GA, Zhilina TN, Kevbrin VV (1999) The alkaliphilic microbial community and its functional diversity. Microbiology 68:503–521

    CAS  Google Scholar 

  11. Rodríguez-Valera F (1988) Characteristics and microbial ecology of hypersaline environments. In: Rodríguez-Valera F (ed) Halophilic bacteria, Ith edn. CRC Press, Boca Raton, FL, pp 3–30

    Google Scholar 

  12. Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544

    PubMed Central  PubMed  CAS  Google Scholar 

  13. Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an athalasso haline lake in Northwestern China. Appl Environ Microbiol 72:3832–3845

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  14. Ghai R, Pašić L, Fernández AB, Martin-Cuadrado AB, Mizuno CM, McMahon KD, Papke RT, Stepanauskas R, Rodriguez-Brito B, Rohwer F, Sánchez-Porro C, Ventosa A, Rodríguez-Valera F (2011) New abundant microbial groups in aquatic hypersaline environments. Sci Rep 1:135

    Article  PubMed Central  PubMed  Google Scholar 

  15. Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci U S A 104:11436–11440

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  16. Canfora L, Bacci G, Pinzari F, Lo Papa G, Dazzi C, Benedetti A (2014) Salinity and bacterial diversity: to what extent does the concentration of salt affect the bacterial community in a saline soil? PLoS One 9:e106662

    Article  PubMed Central  PubMed  Google Scholar 

  17. Dimitriu PA, Pinkart HC, Peyton BM, Mormile MR (2008) Spatial and temporal patterns in the microbial diversity of a meromictic soda lake in Washington State. Appl Environ Microbiol 74:4877–4888

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  18. Pagaling E, Wang H, Venables M, Wallace A, Grant WD, Cowan DA, Jones BE, Ma Y, Ventosa A, Heaphy S (2009) Microbial biogeography of six salt lakes in Inner Mongolia, China, and a Salt Lake in Argentina. Appl Environ Microbiol 75:5750–5760

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  19. Lanzen A, Simachew A, Gessesse A, Chmolowska D, Jonassen I, Ovreas L (2013) Surprising prokaryotic and eukaryotic diversity, community structure and biogeography of Ethiopian soda lakes. PLoS ONE 8:e72577

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  20. Dadheech PK, Glöckner G, Casper P, Kotut K, Mazzoni CJ, Mbedi S, Krienitz L (2013) Cyanobacterial diversity in the hot spring, pelagic and benthic habitats of a tropical soda lake. FEMS Microbiol Ecol 85:389–401

    Article  PubMed  CAS  Google Scholar 

  21. Asao M, Pinkart HC, Madigan MT (2011) Diversity of extremophilic purple phototrophic bacteria in Soap Lake, a central Washington (USA) soda lake. Environ Microbiol 13:2146–2157

    Article  PubMed  CAS  Google Scholar 

  22. de la Haba RR, Arahal DR, Márquez MC, Ventosa A (2010) Phylogenetic relationships within the family Halomonadaceae based on comparative 23S and 16S rRNA gene sequence analysis. Int J Syst Evol Microbiol 60:737–748

    Article  PubMed  Google Scholar 

  23. de la Haba RR, Sanchez-Porro C, Ventosa A (2011) Taxonomy, phylogeny, and biotechnological interest of the family halomonadaceae. In: Ventosa A, Oren A, Ma Y (eds) Halophiles and hypersaline environments. Springer, Heidelbeg, pp 27–64

    Chapter  Google Scholar 

  24. Housh TB, Aranda-Gomez JJ, Luhr JF (2010) Isla Isabel (Nayarit, México): quaternary alkali basalts with mantle xenoliths erupted in the mouth of the Gulf of California. J Volcanol Geotherm Res 197:85–107

    Article  CAS  Google Scholar 

  25. Romero-Viana L, Kienel U, Sasche D (2012) Lipid biomarker signatures in a hypersaline lake on Isabel island (Eastern Pacific) as a proxy for past rainfall anomaly (1942–2006 AD). Palaeogeogr Palaeoclimatol Palaeoecol 350:49–61

    Article  Google Scholar 

  26. Kempers AJ (1974) Determination of sub-microquantities of ammonium and nitrates in soils with phenol, sodium nitroprusside and hypochlorite. Geoderma 12:201–206

    Article  CAS  Google Scholar 

  27. Ramírez-Saad H, Akkermans W, Akkermans ADL (1996) DNA extraction from actinorhizal nodules. Chap. 1.4.4. In: Akkermans ADL, van Elsas JD, de Bruijn F (eds) Manual molecular microbial ecology. Kluwer Academic Publishers, Dordrecht, pp 1–11

    Google Scholar 

  28. Nübel U, Engelen B, Felske A, Snaidr A, Wieshuber A, Amann RI, Ludwig W, Backhaus H (1996) Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol 178:5636–5643

    PubMed Central  PubMed  Google Scholar 

  29. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed Central  PubMed  CAS  Google Scholar 

  30. Ramírez-Saad H, Janse J, Akkermans ADL (1998) Root nodules of Ceanothus caeruleus contain both; the N2-fixing Frankia endophyte and a phylogenetically related Nod−/Fix− actinomycete. Can J Microbiol 44:140–148

    Article  Google Scholar 

  31. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  32. Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319

    Article  PubMed  CAS  Google Scholar 

  33. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  34. Muyzer G, Brinkhoff T, Nübel U, Santegoeds C, Schäfer H, Wawer C (1998) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular microbial ecology manual. Kluwer Academic Publishers, Dordrecht, pp 1–27

    Google Scholar 

  35. Sanguinetti CJ, Dias Nieto E, Simpson AJG (1994) Rapid silver staining and recovery of PCR products separated on polyacrilamyde gels. Biotechniques 17:915–919

    Google Scholar 

  36. Ramírez-Saad HC, Sessitsch A, de Vos WM, Akkermans ADL (2000) Bacterial community changes and enrichment of uncultured Burkholderia-like bacteria induced by chlorinated benzoates in a peat-forest soil-microcosm. Syst Appl Microbiol 23:591–598

    Article  PubMed  Google Scholar 

  37. Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  38. Binladen J, Gilbert MT, Bollback JP, Panitz F, Bendixen C, Nielsen R, Willerslev E (2007) The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS ONE 2(2):e197

    Article  PubMed Central  PubMed  Google Scholar 

  39. Baker G, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555

    Article  PubMed  CAS  Google Scholar 

  40. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  41. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics. doi:10.1093/bioinformatics/btr381

    PubMed Central  PubMed  Google Scholar 

  42. Flynn JM, Brown EA, Chain FJJ, MacIsaac HJ, Cristescu ME (2015) Toward accurate molecular identification of species in complex environmental samples: testing the performance of sequence filtering and clustering methods. Ecol Evol. doi:10.1002/ece3.1497

    PubMed Central  PubMed  Google Scholar 

  43. Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, Schweer T, Peplies J, Ludwig W, Glöckner FO (2014) The SILVA and “all-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Res 42:D643–648

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  44. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  45. Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124

    Article  PubMed Central  PubMed  Google Scholar 

  46. Nguyen NH, Smith D, Peay K, Kennedy P (2015) Parsing ecological signal from noise in next generation amplicon sequencing. New Phytol 205:1389–1393

    Article  PubMed  CAS  Google Scholar 

  47. Antony CP, Kumaresan D, Hunger S, Drake HL, Murrel JC, Shouche YS (2013) Microbiology of Lonar Lake and other soda lakes. ISME J 7:468–476

    Article  PubMed  Google Scholar 

  48. Culkin F, Smith N (1980) Determination of the concentration of potassium chloride solution having the same electrical conductivity, at 15°C and infinite frequency, as standard seawater of salinity 35.0000 ‰ (Chlorinity 19.37394 ‰). IEEE J Ocean Eng 5:22–23

    Article  Google Scholar 

  49. Grant WD (2006) Alkaline environments and biodiversity, in extremophilies. In: Gerday C, Glansdorff N (eds) Encyclopedia of Life Support Systems (EOLSS). Developed under the Auspices of The UNESCO. Eolss Publishers, Oxford, UK

    Google Scholar 

  50. Shapovalova AA, Hizhniak TV, Tourova TP, Muyzer G, Sorokin DY (2009) Halomonas chromatireducens sp. nov., a novel haloalkaliphile from soda soil capable of aerobic chromate reduction. Microbiology (Moscow) 78:117–127

    Article  CAS  Google Scholar 

  51. Bagheri M, Amoozegar MA, Didari M, Makhdoumi-Kakhki A, Schumann P, Spröer C, Sánchez-Porro C, Ventosa A (2013) Marinobacter persicus sp. nov., a moderately halophilic bacterium from a saline lake in Iran. Antonie Van Leeuwenhoek 104:47–54

    Article  PubMed  CAS  Google Scholar 

  52. Nedashkovskaya OI, Kim SB, Vancanneyt M, Shin DS, Lysenko AM, Shevchenko LS, Krasokhin VB, Mikhailov VV, Swings J, Bae KS (2006) Salegentibacter agarivorans sp. nov., a novel marine bacterium of the family flavobacteriaceae isolated from the sponge artemisina sp. Int J Syst Evol Microbiol 56:883–887

    Article  PubMed  CAS  Google Scholar 

  53. Nedashkovskaya OI, Kim SB, Vancanneyt M, Snauwaert C, Lysenko AM, Rohde M, Frolova GM, Zhukova NV, Mikhailov VV, Bae KS, Oh HW, Swings J (2006) Formosa agariphila sp. nov., a budding bacterium of the family Flavobacteriaceae isolated from marine environments, and emended description of the genus Formosa. Int J Syst Evol Microbiol 56:161–167

    Article  PubMed  CAS  Google Scholar 

  54. Bruns A, Rohde M, Berthe-Corti L (2001) Muricauda ruestringensis gen. nov., sp. nov., a facultatively anaerobic, appendaged bacterium from German North Sea intertidal sediment. Int J Syst Evol Microbiol 51:1997–2006

    Article  PubMed  CAS  Google Scholar 

  55. Wani AA, Surakasi VP, Siddharth J, Raghavan RG, Patole MS, Ranade D, Shouche YS (2006) Molecular analyses of microbial diversity associated with the Lonar soda lake in India: an impact crater in a basalt area. Res Microbiol 157:928–937

    Article  PubMed  CAS  Google Scholar 

  56. Wains M, Tindall BJ, Schumann P, lngvorsen K (1999) Gracilibacillus gen. nov., with description of gracilibacillus halotolerans gen. nov., sp. nov.; transfer of bacillus dipsosauri to gracilibacillus dipsosauri comb. nov., and bacillus salexigens to the genus salibacillus gen. nov., as salibacillus salexigens comb. nov. Int J Syst Evol Microbiol 49:821–831

    Google Scholar 

  57. Rees HC, Grant WD, Jones BE, Heaphy S (2003) Diversity of Kenyan soda Lake alkaliphiles assessed by molecular methods. Extremophiles 8:63–71

    Article  PubMed  Google Scholar 

  58. Desnues C, Michotey VD, Wieland A, Zhizang C, Fourcans A, Duran R, Bonin PC (2007) Seasonal and dial distributions of denitrifying and bacterial communities in a hypersaline microbial mat (Camargue, France). Water Res 41:3407–3419

    Article  PubMed  CAS  Google Scholar 

  59. Foti MJ, Sorokin DY, Zacharova EE, Pimenov NV, Gijs Kuenen JG, Muyzer G (2008) Bacterial diversity and activity along a salinity gradient in soda lakes of the Kulunda Steppe (Altai, Russia). Extremophiles 12:133–145

    Article  PubMed  CAS  Google Scholar 

  60. Sorokin DY, van Pelt S, Tourov TP, Evtushenko LI (2009) Nitriliruptor alkaliphilus gen. nov., sp. nov., a deep-lineage haloalkaliphilic actinobacterium from soda lakes capable of growth on aliphatic nitriles, and proposal of nitriliruptoraceae fam. nov. and nitriliruptorales ord. nov. Int J Syst Evol Microbiol 59:248–253

    Article  PubMed  CAS  Google Scholar 

  61. Weon HY, Kim BY, Yoo SH, Kim JS, Kwon SW, Go SJ, Stackebrandt E (2006) Loktanella koreensis sp. nov., isolated from sea sand in Korea. Int J Syst Evol Microbiol 56:2199–2202

    Article  PubMed  CAS  Google Scholar 

  62. Yoon JH, Kang SJ, Lee SY, Jung YT, Lee JS, Oh TK (2012) Marivita hallyeonensis sp. nov., isolated from seawater, reclassification of Gaetbulicola byunsanensis as Marivita byunsanensis comb. nov. and emended description of the genus Marivita Hwang et al. Int J Syst Evol Microbiol 62:839–843

    Article  PubMed  CAS  Google Scholar 

  63. WoRMS Editorial Board (2015) World register of marine species. Available from http://www.marinespecies.org at VLIZ

Download references

Acknowledgments

This work was supported by research grants CSD 2009–0006 of the Consolider-Ingenio programme and BIO2014-51953-P from the Spanish Ministerio de Ciencia e Innovación, currently the Ministerio de Economía y Competitividad, all including ERDF (European Regional Development Funds). JFAG was supported by a postdoctoral fellowship from CONACyT (Mexico). We wish to thank referees for their constructive commentaries which improved the manuscript.

Conflict of Interest

All authors declare no conflict of interest in this manuscript

Author information

Authors and Affiliations

  1. Grupo de Ecología Genética, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, C/ Profesor Albareda 1, 18008, Granada, Spain

    José Félix Aguirre-Garrido, Nicolás Toro & Francisco Martínez-Abarca

  2. Departamento de Sistemas Biológicos, Universidad Autónoma Metropolitana, Unidad Xochimilco, Calz. del Hueso 1110, CP 14310, DF México, Mexico

    José Félix Aguirre-Garrido & Hugo César Ramírez-Saad

Authors
  1. José Félix Aguirre-Garrido
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hugo César Ramírez-Saad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolás Toro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francisco Martínez-Abarca
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francisco Martínez-Abarca.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 30 kb)

Figure S1

Location of Isabel Island in the Pacific coast of Mexico. Shape of Isabel Island and the crater-lake draw at scale. Sampling sites (1–3) for water and sediment collection are indicated by arrowheads\ (GIF 23 kb)

High resolution image (TIFF 43 kb)

Figure S2

Bacterial diversity in Isabel soda-lake samples. Rarefaction analysis was based on Operational Taxonomic Units (OTU’s) established at 97 % sequence identity of partial 16S rRNA gene sequences of water and sediment samples from Isabel Island Lake (GIF 12 kb)

High resolution image (TIFF 335 kb)

Figure S3

16S rRNA gene fingerprint of γ-Proteobacteria isolates from Isabel Island lake samples. Total DNA of selected isolates was digested, electrophoresed and vacuum-blotted onto nylon filters. A PCR fragment (340 bp) of Halomonas venusta (4WSA1) 16S rRNA gene was used as probe. Hybridization fingerprints point to different number of rrn operons (ranging from 2 to 5) according to the genus. Positions of DNA molecular size markers (kbp) are shown on left side (GIF 71 kb)

High resolution image (TIFF 210 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aguirre-Garrido, J.F., Ramírez-Saad, H.C., Toro, N. et al. Bacterial Diversity in the Soda Saline Crater Lake from Isabel Island, Mexico. Microb Ecol 71, 68–77 (2016). https://doi.org/10.1007/s00248-015-0676-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-015-0676-6

Keywords

Search

Navigation