Diversity of culturable thermo-resistant aquatic bacteria along an environmental gradient in Cuatro Ciénegas, Coahuila, México

Antonie van Leeuwenhoek, International Journal of General and Molecular Microbiology

Volumn 99, Issue 2, 2011, Pages 303-318

  Cerritos, René ^a,b   Eguiarte, Luis E ^a   Avitia, Morena ^a   Siefert, Janet ^c   Travisano, Michael ^d   Rodríguez Verdugo, Alejandra ^a,e   Souza, Valeria ^a  

^a INSTITUTO DE ECOLOGÍA   (Mexico)

^b INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^c RICE UNIVERSITY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Actinobacteria; Bacillus; Bacterial diversity; Churince; Desert; Firmicutes; Local diversification; M xico

Indexed keywords

BACTERIAL DNA; DISSOLVED OXYGEN; RNA 16S; SODIUM; SURFACE WATER;

ACTINOBACTERIA; ARTICLE; BACILLUS; BACILLUS CEREUS; BACILLUS FORAMINIS; BACILLUS LIQUENIFORMIS; BACILLUS PUMILUS; BACTERIUM ISOLATE; BACTERIUM ISOLATION; CLADISTICS; CONTROLLED STUDY; DNA EXTRACTION; ENVIRONMENTAL FACTOR; FIRMICUTES; HALOBACILLUS; HALOBACILLUS LITORALIS; HEAT TOLERANCE; HYDROLOGY; MEXICO; MICROCOCCUS LUTEUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RNA SEQUENCE; SALINITY; SPECIES DISTRIBUTION; SPECIES DIVERSITY; STRAIN DIFFERENCE; UNINDEXED SEQUENCE; WATER SAMPLING; WATER TEMPERATURE;

BIODIVERSITY; CLUSTER ANALYSIS; DNA FINGERPRINTING; DNA, BACTERIAL; DNA, RIBOSOMAL; GRAM-POSITIVE BACTERIA; MEXICO; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; TEMPERATURE; WATER MICROBIOLOGY;

ACTINOBACTERIA; ANIMALIA; BACILLARIOPHYTA; BACILLUS (BACTERIUM); BACTERIA (MICROORGANISMS); FIRMICUTES; GASTROPODA; PISCES;

EID: 79952429285     PISSN: 00036072     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10482-010-9490-9     Document Type: Article

References (56)

1. LD Alcaraz G Olmedo G Bonilla R Cerritos G Hernández A Cruz E Ramírez C Putonti B Jiménez E Martinez V López JL Arvizu F Ayala F Razo J Caballero J Siefert L Eguiarte J-P Vielle O Martinez V Souza A Herrera-Estrella L Herrera-Estrella 2008 The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment Proc Natl Acad Sci USA 105 5803 5808 1:CAS:528:DC%2BD1cXltFShsbs%3D 10.1073/pnas.0800981105 18408155 (Pubitemid 351758453)
2. Alcaraz LD, Moreno-Hagelsieb G, Souza V, Herrera-Estrella L, Olmedo G (2010) Understanding the evolutionary relationships and major traits of Bacillus through comparative genomics. BMC Genomics. http://www.biomedcentral.com/1471- 2164/11/332
3. Badino G, Bernabei T, De Vivo A, Giulivo I, Savino G (2004) Under the desert: the mysterious waters of Cuatro Ciénegas, 1st edn. Italy Associazione geografica La Venta, Treviso
4. DL Balkwill JK Fredrickson JM Thomas 1989 Vertical and horizontal variations in the physiological diversity of the aerobic chemoheterotrophic bacterial microflora in deep southeast coastal plain subsurface sediment Appl Environ Microbiol 55 1058 1065 1:STN:280:DC%2BC3crotFektw%3D%3D 16347902
5. S Benlloch A López-López E Casamayor LO ∅vreås V Goddard L Daae Frida G Smerdon R Massana I Joint F Thingstad C Pedrós-Alió F Rodríguez-Valera 2002 Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern Environ Microbiol 4 349 360 10.1046/j.1462-2920.2002.00306.x 12071980 (Pubitemid 34788807)
6. EW Carson TE Dowling 2006 Influence of hydrogeographic history and hybridization on the distribution of genetic variation in the pupfishes Cyprinodon atrorum and C Mol Ecol 15 667 679 1:CAS:528:DC%2BD28XjsVGnsLk%3D 10.1111/j.1365-294X.2005.02763.x 16499693 (Pubitemid 43344784)
7. E Casamayor J Calderon-Paz C Pedrós Alió 2004 5S rRNA fingerprints of marine bacteria, halophilic archaea and natural prokariotic assemblages along a salinity gradient FEMS Microbiol Ecol 34 113 119
8. Cerritos R (2008) Análisis de concepto biológico, ecológico, cohesivo y filogenético de especie en bacterias halófilas del valle de Cuatro Ciénegas, Coahuila. PhD Thesis, Instituto de Ecología UNAM, México
9. R Cerritos P Vinuesa L Eguiarte L Herrera-Estrella L Alcaraz-Peraza J Arvizu-Gómez G Olmedo E Ramirez J Siefert V Souza 2008 Bacillus coahuilensis sp. nov. a new moderately halophilic species from pond in the Cuatro Ciénegas Valley in Coahuila, México Int J Syst Evol Microbiol 58 919 923 1:CAS:528:DC%2BD1cXmtlSitbw%3D 10.1099/ijs.0.64959-0 18398195
10. P Chaturvedi S Shivaji 2006 Exiguobacterium indicum sp. nov., a psychrophilic bacterium from the Hamta glacier of the Himalayan mountain ranges of India Int J Syst Evol Microbiol 56 Pt 12 2765 2770 1:CAS:528: DC%2BD2sXhtVWmsbw%3D 10.1099/ijs.0.64508-0 17158975 (Pubitemid 44970985)
11. F Cohan 2003 What are bacterial species? Annu Rev Microbiol 56 457 458 10.1146/annurev.micro.56.012302.160634
12. BC Crump C Hopkinson M Sogin JE Hobbie 2004 Microbial biogeography along an estuarine salinity gradient: combined influences of bacterial growth and residence time Appl Environ Microbiol 70 1494 1505 1:CAS:528: DC%2BD2cXisVKju7g%3D 10.1128/AEM.70.3.1494-1505.2004 15006771 (Pubitemid 38365131)
13. Winsborough BM, Theriot E, Czarnecki, DB (2008) Diatoms on a continental "island": Lazarus species, marine disjuncts and other endemic diatoms of the Cuatro Ciénegas basin, Coahuila, México. University of Texas, 257 pp
14. D Dean-Ross AL Mills 1989 Bacterial community structure and function along a heavy metal gradient Appl Environ Microbiol 55 2002 2009 1:CAS:528:DyaL1MXltlSls7Y%3D 16347991
15. L Demergasso E Casamayor G Chong P Galleguillos L Escudero C Pedrós-Alió 2004 Distribution of prokaryotic genetic diversity in athalassohaline lakes of the Atacama desert Northern Chile FEMS Microbiol Ecol 48 57 69 1:CAS:528:DC%2BD2cXisF2gt74%3D 10.1016/j.femsec.2003.12.013 19712431 (Pubitemid 38393776)
16. C Desnues B Rodriguez-Brito S Rayhawk S Kelley T Tran M Haynes H Liu M Burlan L Wegley B Chau Y Ruan D Hall FE Angly RA Edwards L Li RV Thurber RP Reid J Siefert V Souza DL Valentine BK Swan M Breitbart F Rohwer 2008 Biodiversity and biogeography of phages in modern stromatolites and thrombolites Nature 452 340 343 1:CAS:528:DC%2BD1cXjsFCnsLs%3D 10.1038/nature06735 18311127 (Pubitemid 351430793)
17. AM Earl R Losick R Kolter 2007 Bacillus subtilis genome diversity J Bacteriol 189 1163 1170 1:CAS:528:DC%2BD2sXht1ehu7w%3D 10.1128/JB.01343-06 17114265 (Pubitemid 46183894)
18. JJ Elser JH Schambel M Kyle J Watts EW Carson TE Dowling C Tang PD Roopnarine 2005 Response of grazing snails to phosphorus enrichment of modern stromatolitic microbial communities Freshw Biol 50 1808 1825 1:CAS:528:DC%2BD2MXht1CgsLvO 10.1111/j.1365-2427.2005.01451.x (Pubitemid 43906866)
19. AE Escalante LE Eguiarte L Espinosa-Asuar LJ Forney AM Noguez V Souza 2008 Diversity of aquatic prokaryotic communities in the Cuatro Ciénegas basin FEMS Microbiol Ecol 65 50 60 1:CAS:528:DC%2BD1cXotlKgtL8%3D 10.1111/j.1574-6941.2008.00496.x 18479448 (Pubitemid 351832103)
20. E Escalante J Caballero-Mellado L Martinez-Aguilar A Rodriguez-Verdugo A Gonzalez-Gonzalez J Toribio-Jimenez V Souza 2009 Pseudomonas cuatrociénegasensis sp. nov., isolated from an evaporating lagoon in the Cuatro Ciénegas valley in Coahuila, México Int J Syst Evol Microbiol 59 1416 1420 1:CAS:528:DC%2BD1MXos1Ciur0%3D 10.1099/ijs.0.006189-0 19502326
21. TA Hall 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT Nucleic Acids Symp Ser 41 95 98 1:CAS:528:DC%2BD3cXhtVyjs7Y%3D
22. C Hubert A Loy M Nickel C Arnosti C Baranyi V Bruchert T Ferdelman K Finster F Mønsted Christensen JR Rezende V Vandieken BB Jørgensen 2009 Into the cold arctic seabed a constant flux of diverse thermophilic bacteria Science 325 1541 1:CAS:528:DC%2BD1MXhtFanurrJ 10.1126/science.1174012 19762643
23. JP Huelsenbeck FR Ronquist 2001 MrBayes: Bayesian inference of phylogenetic trees Bioinformatics 17 754 755 1:STN:280:DC%2BD3MvotV2isw%3D%3D 10.1093/bioinformatics/17.8.754 11524383 (Pubitemid 32851390)
24. CA Istock KE Duncan N Ferguson X Zhou 1992 Sexuality in a natural population of bacteria-Bacillus subtilis challenges the clonal paradigm Mol Ecol 1 95 103 1:STN:280:DyaK2c3js1akuw%3D%3D 10.1111/j.1365-294X.1992.tb00161.x 1344989
25. S Jiang W Sun M Chen S Dai L Zhang Y Liu KJ Lee X Li 2007 Diversity of culturable actinobacteria isolated from marine sponge Haliclona sp Antonie van Leeuwenhoek 92 405 416 1:CAS:528:DC%2BD2sXhtVyntbzL 10.1007/s10482-007-9169-z 17566868 (Pubitemid 47500375)
26. HK Johannesson A Cortés KC Kilroy 2004 Reconnaissance isotopic and hydrochemical study of Cuatro Ciénegas groundwater, Coahuila, México South Am Earth Sci 17 171 180 10.1016/j.jsames.2004.01.002 (Pubitemid 39437028)
27. SG Johnson 2005 Age, phylogeography and population structure of the microendemic banded spring snail, Mexipyrgus churinceanus Mol Ecol 14 2299 2311 1:CAS:528:DC%2BD2MXmvF2qsLw%3D 10.1111/j.1365-294x.2005.02580.x 15969715 (Pubitemid 40886032)
28. H Kaartokallio M Laamanen K Sivonen 2005 Responses of Baltic sea ice and open-water natural bacterial communities to salinity change Appl Environ Microbiol 71 4364 4371 1:CAS:528:DC%2BD2MXoslGitLg%3D 10.1128/AEM.71.8.4364- 4371.2005 16085826 (Pubitemid 41129489)
29. MJ Laamenem L Forsström K Sivonen 2002 Diversyty of Aphanizomenom flos-aquae (Cyanobacterium) populations along a Baltic sea salinity gradient Appl Environ Microbiol 68 5296 5303 10.1128/AEM.68.11.5296-5303.2002 (Pubitemid 35265660)
30. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic acid techniques. In: Strackebrant E, Goodfellow M (eds) Bacterial systematics. Wiley, New York, NY, pp 115-175
31. B Larget DL Simon 1999 Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees Mol Biol Evol 16 750 759 1:CAS:528:DyaK1MXjslGitb8%3D (Pubitemid 29260829)
32. Ludwig JA, Reynolds JF (1998) Principal component analysis. In: Ludwig JA, Reynolds JF (eds) Statitistical ecology. A primer on methods, computing. Wiley, New York, NY, pp 223-241
33. PA Maron DPH Lejon E Carvalho K Bizet P Lemanceau L Ranjard C Mougel 2005 Assessing genetic structure and diversity of airborne bacterial communities by DNA fingerprinting and 16S rDNA clone library Atmos Environ 39 3687 3695 1:CAS:528:DC%2BD2MXlt1WmsLo%3D 10.1016/j.atmosenv.2005.03.002 (Pubitemid 40834277)
34. ER Meyer 1973 Late-quaternary paleoecology of the Cuatro Ciénegas basin, Coahuila, México Ecology 54 982 995 10.2307/1935565
35. TA Minckley ST Jackson 2008 Ecological stability in a changing world? Reassessment of the paleoenvironmental history of Cuatro Ciénegas, México J Biogeogr 35 188 190 10.1111/j.1365-2699.2007.01829.x (Pubitemid 350258490)
36. WL Minkley 1984 Cuatro Ciénegas fishes: research review of a local test of diversity vesus habitat size Arizona-Nevada Acad Sci 19 13 21
37. S Porwal LS Cheema VC Kalia 2009 Phylogeny in aid of the present and novel microbial lineages: diversity in Bacillus PLoS ONE 4 2 4438 10.1371/journal.pone.0004438
38. Rademaker JL, de Brujin FJ (1998) Characterization and classification of microbes by rep-PCR genomic fingerprinting and computer assisted pattern analysis. In: Akkermans ADL, van Elsas JE, de Brujin FJ (eds) Molecular ecology manual. Kluwer Academic Publishers, Dordrecht, pp 157-159
39. HC Rees WD Grant BE Jones S Heaphy 2004 Diversity of Kenyan soda lake alkaliphiles assessed by molecular methods Extremophiles 8 63 71 1:CAS:528:DC%2BD2cXos1ertw%3D%3D 10.1007/s00792-003-0361-4 15064991 (Pubitemid 40882703)
40. M Roebler V Müller 1998 Quantitative and physiological analyses of chloride dependence of growth of Halobacillus halophilus Appl Environ Microbiol 64 3813 3817 (Pubitemid 28462977)
41. Rohlf JF (1998) NTSYS-pc numerical taxonomy and multivariate analysis system (2.02c). Exeter Publishing, USA
42. CT Sacchi AM Whitney LW Mayer R Morey A Steigerwalt A Boras RS Weyant T Popovic 2002 Sequencing of 16S rRNA gene: a rapid tool for identification of Bacillus anthracis Emerg Infect Dis 8 1117 1123 1:CAS:528:DC%2BD38XoslWnt78%3D 12396926 (Pubitemid 35257004)
43. SAS (2005) Institute. Cary, NC, USA
44. V Souza L Espinoza-Asuar AE Escalante LE Eguiarte J Farmer L Forney L Lloret JM Rodríguez-Martinez J Soberon R Dirzo JJ Elser 2006 An endangered oasis of aquatic microbial diversity in the Chihuahuan desert Proc Nat Acad Sci USA 17 6565 6570 10.1073/pnas.0601434103
45. V Souza LE Eguiarte J Siefert JJ Elser 2008 Microbial endemism: does phosphorous limitations enhance speciation? Nat Rev Microbiol 6 559 564 1:CAS:528:DC%2BD1cXntFOrtrk%3D 10.1038/nrmicro1917 18521074 (Pubitemid 351850979)
46. S Spring W Ludwig MC Marquez A Ventosa KH Schleifer 1996 Halobacillus gen. nov. with descriptions of Halobacillus litoralis sp. nov. and Halobacillus trueperi sp. nov., and transfer of Sporosarcina halophila to Halobacillus halophilus comb. nov Int J Syst Bacteriol 46 492 496 10.1099/00207713-46-2-492 10.1099/00207713-46-2-492 (Pubitemid 26113875)
47. E Stackebrandt BM Goebel 1994 Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology Int J Syst Bacteriol 44 846 849 1:CAS:528:DyaK2MXitFCnsb4%3D 10.1099/00207713-44-4-846 (Pubitemid 24315169)
48. E Stackebrandt W Frederiksen JM Garrity PAD Grimont P Kampfer CJM Maiden X Nesme R Rosello-Mora J Swings, et al. 2002 Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology Int J Syst Evol Microbiol 52 1043 1047 1:CAS:528:DC%2BD38XkslCqs7g%3D 10.1099/ijs.0.02360-0 12054223 (Pubitemid 34591239)
49. JT Staley JJ Gosink 1999 Poles apart: biodiversity and biogeography of sea ice bacteria Annu Rev Microbiol 53 189 215 1:CAS:528:DyaK1MXmvVOnsLg%3D 10.1146/annurev.micro.53.1.189 10547690 (Pubitemid 29503730)
50. A Szynkiewicza C Ryan C Ewing H Craig MG Moorea D Bustose LM Pratta 2009 Origin of terrestrial gypsum dunes-implications for Martian gypsum-rich dunes of Olympia Undae Geomorphology 121 69 83 10.1016/j.geomorph.2009.02.017
51. DW Taylor 1966 A remarkable snail fauna from Coahuila, México Veliger 9 152 228
52. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins 1997 The ClustalX Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 24 4876 4882 10.1093/nar/25.24.4876 (Pubitemid 28022245)
53. I Tiago AN Chung A Verissimo 2004 Bacterial diversity in a nonsaline alkaline environment heterotrophic aerobic populations Appl Environ Microbiol 70 7378 7387 1:CAS:528:DC%2BD2cXhtFaitrjO 10.1128/AEM.70.12.7378-7387.2004 15574939 (Pubitemid 39643804)
54. M Tobler EW Carson 2010 Environmental variation, hybridization, and phenotypic diversification in Cuatro Ciénegas pupfhes J Evol Biol 23 1475 1489 1:STN:280:DC%2BC3cnot1CgsQ%3D%3D 10.1111/j.1420-9101.2010.02014.x 20524951
55. P Vinuesa JL Rademaker FJ de Brujin D Werner 1998 Genotypic characterization of Brayrhizobium strains nodulating endemic woody legumes of the Canary Island by PCR- restriction fragment length polymorphism analysis of genes encoding 16S rRNA (16S rRNA) and 16S-23S rRNA intergenic spacers, repetitive extragenic palindromic PCR genomic fingerprinting and partial 16S rRNA sequencing Appl Environ Microbiol 64 2096 2104 1:CAS:528:DyaK1cXjslWhsLk%3D 9603820 (Pubitemid 28252770)
56. JH Yoon IG Kim KH Kang TK Oh YH Park 2003 Bacillus marisflavi sp. nov. and Bacillus aquimaris sp. nov., isolated from sea water of a tidal flat of the Yellow sea in Korea Int J Sys Evol Microbiol 53 1297 1303 1:CAS:528: DC%2BD3sXotlymu7s%3D 10.1099/ijs.0.02365-0 (Pubitemid 37184958)