Abstract
Microbial communities are responsible for important ecosystem processes, and their activities are regulated by environmental factors such as temperature and solar ultraviolet radiation. Here we investigate changes in aquatic microbial community structure, diversity, and evenness in response to changes in temperature and UV radiation. For this purpose, 15 mesocosms were seeded with both microbial mat communities and plankton from natural pools within the Cuatro Cienegas Basin (Mexico). Clone libraries (16S rRNA) were obtained from water samples at the beginning and at the end of the experiment (40 days). Phylogenetic analysis indicated substantial changes in aquatic community composition and structure in response to temperature and UV radiation. Extreme treatments with elevation in temperature or UV radiation reduced diversity in relation to the Control treatments, causing a reduction in richness and increase in dominance, with a proliferation of a few resistant operational taxonomic units. Each phylum was affected differentially by the new conditions, which translates in a differential modification of ecosystem functioning. This suggests that the impact of environmental stress, at least at short term, will reshape the aquatic bacterial communities of this unique ecosystem. This work also demonstrates the possibility of designing manageable synthetic microbial community ecosystems where controlled environmental variables can be manipulated. Therefore, microbial model systems offer a complementary approach to field and laboratory studies of global research problems associated with the environment.
Similar content being viewed by others
References
Adams HE, Crump BC, Kling GW (2010) Temperature controls on aquatic bacterial production and community dynamics in arctic lakes and streams. Environ Microbiol 12:1319–1333
Alcaraz LD, Olmedo G, Bonilla G, Cerritos R, Hernández G (2008) The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment. Proc Natl Acad Sci U S A 105:5803–5808
Alonso-Sáez L, Gasol JM, Lefort T, Hofer J, Sommaruga R (2006) Effect of natural sunlight on bacterial activity and differential sensitivity of natural bacterioplankton groups in northwestern Mediterranean coastal waters. Appl Environ Microbiol 72:5806–5813
Arrieta JM, Weinbauer MG, Herndl G (2000) Interspecific variability in sensitivity to UV radiation and subsequent recovery in selected isolates of marine bacteria. Appl Environ Microbiol 66:1468–1473
Azam F, Malfatti F (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5:782–791
Bell T, Newman JA, Silverman BW, Turner SL, Lilley AK (2005) The contribution of species richness and composition to bacterial services. Nature 436:1157–1160
Bentley SD, Parkhill J (2004) Comparative genomic structure of prokaryotes. Annu Rev Genet 38:771–791
Bertilsson S, Eiler A, Nordqvist A, Jørgensen NOG (2007) Links between bacterial production, amino-acid utilization and community composition in productive lakes. ISME J 1:532–544
Breitbart M, Hoare A, Nitti A et al (2009) Metagenomic and stable isotopic analyses of modern freshwater microbialites in Cuatro Cienegas, Mexico. Environ Microbiol 11:16–34
Callieri C (2007) Picophytoplankton in freshwater ecosystems: the importance of small-sized phototrophs. Freshwat Rev 1:1–28
Cavicchioli R, Ostrowski M, Fegatella F, Goodchild A, Guixa-Boixereu N (2003) Life under nutrient limitation in oligotrophic marine environments: an eco/physiological perspective of Sphingopyxis alaskensis (formerly Sphingomonas alaskensis). Microb Ecol 45:203–217
Cerritos R, Eguiarte LE, Avitia M et al (2011) Diversity of culturable thermo-resistant aquatic bacteria along an environmental gradient in Cuatro Cienegas, Coahuila, Mexico. Antonie Van Leeuwenhoek 99:303–318
Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing compositional similarity based on incidence and abundance data. Ecol Lett 8:148–159
DeSantis TZ, Dubosarskiy I, Murray SR, Andersen GL (2003) Comprehensive aligned sequence construction for automated design of effective probes (CASCADE-P) using 16S rDNA. Bioinformatics 19:1461–1468
Desnues C, Rodriguez-Brito B, Rayhawk S et al (2008) Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452:340–343
Escalante AE, Eguiarte LE, Espinosa L et al (2008) Diversity of aquatic prokaryotic communities in the Cuatro Cienegas basin. FEMS Microbiol Ecol 65:50–60
Fuchs BM, Spring S, Teeling H et al (2007) Characterization of a marine gammaproteobacterium capable of aerobic anoxygenic photosynthesis. Proc Natl Acad Sci U S A 104:2891
Fuerst JA, Hawkins JA, Holmes A et al (1993) Porphyrobacter neustonensis gen. nov., sp. nov., an aerobic bacteriochlorophyll-synthesizing budding bacterium from fresh water. Int J Syst Bacteriol 43:125–134
García-Pichel F (1994) A model for the internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreens. Limnol Oceanogr 39:1704–1717
Glöckner FO, Zaichikov E, Belkova N et al (2000) Comparative 16S rRNA analysis of lake bacterioplankton reveals globally distributed phylogenetic clusters including an abundant group of actinobacteria. Appl Environ Microbiol 66:5053–5065
González JM, Fernández-Gómez B, Fernández-Guerra A et al (2008) Genome analysis of the proteorhodospin-containing marine bacterium Polaribacter sp. Proc Natl Acad Sci U S A 105:8724–8729
Green SJ, Jahnke LL (2010) Molecular investigations and experimental manipulations of microbial mats: a view to paleomicrobial ecosystems. In: Seckbach J, Oren A (eds) Microbial mats: modern and ancient microorganisms in stratified systems. Springer, Berlin, pp 185–208
Hahn MW (2009) Description of seven candidate species affiliated with the phylum Actinobacteria, representing planktonic freshwater bacteria. IJSEM 59:112–117
Hahn MW, Lünsdorf H, Wu Q et al (2003) Isolation of novel ultramicrobacteria classified as Actinobacteria from five freshwater habitats in Europe and Asia. Appl Environ Microbiol 69:1442–1451
Hisada T, Okamura K, Hiraishi A (2007) Isolation and characterization of phototrophic purple nonsulfur bacteria from Chloroflexus and cyanobacterial mats in hot springs. Microbes Environ 22:405–411
Hoehler TM, Bebout BM, Des Marais DJ (2001) The role of microbial mats in the production of reduced gases on the early Earth. Nature 412:324–327
Hughes JB, Hellmann JJ (2005) The application of rarefaction techniques to molecular inventories of microbial diversity. Meth Enzymol 397:292–308
Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJ (2001) Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67:4399–4406
Hutalle-Schmelzer KM, Zwirnmann E, Krüger A, Grossart HP (2010) Enrichment and cultivation of pelagic bacteria from a humic lake using phenol and humic matter additions. FEMS Microbiol Ecol 72:58–73
Imhoff JF (2005) The Proteobacteria, part C. The Alphaproteobacteria family I. Rhodospirillaceae. In: Brenner DJ, Kreig NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, p 32
Jagger J (1983) Physiological effects of near-ultraviolet radiation on bacteria. Photochem Photobiol Rev 7:1–75
Jessup CM, Kassen R, Forde SE et al (2004) Big questions, small worlds: microbial model systems in ecology. Trends Ecol Evol 19:189–197
Joux F, Jeffrey WH, Lebaron P, Mitchell DL (1999) Marine bacterial isolates display diverse responses to UVB radiation. Appl Environ Microbiol 65:3820–3827
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackenbrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–157
Lauro FM, McDougald D, Thomas T et al (2009) The genomic basis of thropic strategy in marine bacteria. Proc Natl Acad Sci U S A 106:15527–15533
Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinform 23:127–128
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76
Mackenzie C, Chidambaram M, Sodergren EJ, Kaplan S, Weinstock GM (1995) DNA repair mutants of Rhodobacter sphaeroides. J Bacteriol 177:3027–3035
Magurran AE (2004) Measuring biological diversity. Blackwell, Oxford, 256 p
Minckley W (1969) Environments of the Bolson of Cuatro Cienegas, Cuahuila, Mexico, with special reference to the aquatic biota. University of Texas, El Paso. Science Series 2:1–65
Moreno-Letelier A, Olmedo G, Eguiarte LE, Martínez-Castilla L, Souza V (2011) Parallel evolution and horizontal gene transfer of the pst operon in Bacillus from oligotrophic environments. Int J Evol Biol. doi:10.4061/2011/781642
Newton RJ, Jones SE, Eiler A, McMahon KD, Bertilsson S (2011) A guide to the natural history of freshwater lake bacteria. Microbiol Mol Biol Rev 75:14–49
Nübel U, García-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332
Ordoñez OF, Flores MR, Dib JR, Paz A, Farías ME (2009) Extremophile culture collection from Andean lakes: extreme pristine environments that host a wide diversity of microorganisms with tolerance to UV radiation. Microb Ecol 58:461–473
Ostrowski M, Cavicchioli R, Blaauw M, Gottschal JC (2001) Specific growth rate plays a critical role in hydrogen peroxide resistance of the marine oligotrophic ultramicrobacterium Sphingomonas alaskensis strain RB2256. Appl Environ Microbiol 67:1292–1299
Pedrós-Alió C (2006) Marine microbial diversity: can it be determined? Trends Microbiol 14:257–263
Peimbert M, Alcaraz LD, Hernández I et al (2012) Extreme Redfield ratios, metagenomic and microbial diversity analyses of a seasonal shallow red pool in Cuatro Cienegas Coahuila, Mexico. Astrobiology (in press)
Pettersson M, Baath E (2003) The rate of change of a soil bacterial community after liming as a function of temperature. Microb Ecol 46:177–186
Philosof A, Sabehi G, Béjà O (2009) Comparative analyses of actinobacterial genomic fragments from Lake Kinneret. Environ Microbiol 11:3189–3200
Rényi A (1961) On measures of information and entropy. In: Proc 4th Berkeley Symp on Math, Statist Prob. Univ California, pp 547–561
Ross JC, Vincent WF (1998) Temperature dependence of UV radiation effects on antarctic cyanobacteria. J Phycol 34:118–125
Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Sharma AK, Sommerfeld K, Bullerjahn GS et al (2009) Actinorhodopsin genes discovered in diverse freshwater habitats and among cultivated freshwater Actinobacteria. ISME J 3:726–737
Souza V, Eguiarte LE, Siefert J, Elser JJ (2008) Microbial endemism: does phosphorus limitation enhance speciation? Nat Rev Microbiol 6:559–564
Souza V, Espinosa-Asuar L, Escalante AE et al (2006) An endangered oasis of aquatic microbial biodiversity in the Chihuahuan desert. Proc Natl Acad Sci U S A 103:6565–6570
Souza V, Siefert J, Escalante AE, Elser JJ, Eguiarte LE (2012) The Cuatro Cienegas Bolson in Coahuila, Mexico: an astrobiological Precambrian park. Astrobiology (in press)
Szabo KE, Itor POB, Bertilsson S, Tranvik L, Eiler A (2007) Importance of rare and abundant populations for the structure and functional potential of freshwater bacterial communities. Aquat Microb Ecol 47:1–10
Tobler M, Carson EW (2010) Environmental variation, hybridization, and phenotypic diversification in Cuatro Cienegas pupfishes. J Evol Biol 23:1475–1489
Vincent WF, Quesada A (1997) Microbial niches in the polar environment and the escape from UV radiation in non-marine habitats. In: Battaglia B, Valencia J, Walton D (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 388–395
Warnecke F, Amann R, Pernthaler J (2004) Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environ Microbiol 6:242–253
Warnecke F, Sommaruga R, Sekar R, Hofer JS, Pernthaler J (2005) Abundances, identity, and growth state of Actinobacteria in mountain lakes of different UV transparency. Appl Environ Microbiol 71:5551–5559
Winter C, Moeseneder MM, Herndl GJ (2001) Impact of UV radiation on bacterioplankton community composition. Appl Environ Microbiol 67:665–672
Yabuuchi E, Kosako Y (2005) Order IV. Sphingomonadales ord. nov. In: Brenner DJ, Kreig NR, Staley JT, Garrity GM (eds) Bergey’s manual of systematic bacteriology, vol 2, 2nd edn. Springer, New York, pp 230–233
Zwart G, Crump BC, Agterveld MPKW, Hagen F, Han SK (2002) Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol 28:141–155
Acknowledgments
This work was done with the grants to VS: SEP CONACyT 50705, SEMARNAT 0023459. and WWF-Alianza Carlos Slim OL039. SP had a postdoctoral scholarship from CSIC (Spain). VS and LEE worked on the manuscript during their sabbatical leave with a DGAPA support for VS and LEE and UC-Mexus/Conacyt support for LEE. We thank particularly R. González Chauvet, M. Rodríguez, C. Alonso, and A. Uscanga, as well as people from the Molecular and Experimental Evolution Laboratory (UNAM) for the technical assistance in the field, L. Espinosa Asuar for the technical assistance in the laboratory, L. Falcón for the methodological advise, and C. Rooks for reading the manuscript. We specially thank PRONATURA Noreste for the access to the Pozas Azules ranch, the office of APFF of Cuatro Cienegas for their constant support, and the Hotel Marielena for providing long-term housing and support for the experiment.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pajares, S., Bonilla-Rosso, G., Travisano, M. et al. Mesocosms of Aquatic Bacterial Communities from the Cuatro Cienegas Basin (Mexico): A Tool to Test Bacterial Community Response to Environmental Stress. Microb Ecol 64, 346–358 (2012). https://doi.org/10.1007/s00248-012-0045-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-012-0045-7