Alternative states drive the patterns in the bacterioplankton composition in shallow Pampean lakes (Argentina).

We assessed the influence of environmental factors in shaping the free-living bacterial community structure in a set of shallow lakes characterized by contrasting stable state patterns (clear-vegetated, inorganic-turbid and phytoplankton-turbid). Six temperate shallow lakes from the Pampa Plain (Argentina) were sampled over an annual cycle, and two fingerprinting techniques were applied: a 16S rDNA analysis was performed using denaturing gradient gel electrophoresis (DGGE) profiles, and a 16S-23S internally transcribed spacer region analysis was conducted by means of automated ribosomal intergenic spacer analysis (ARISA) profiles. Our results show that the steady state that characterized the different shallow lakes played a major role in structuring the community: the composition of free-living bacteria differed significantly between clear-vegetated, inorganic-turbid and phytoplankton-turbid shallow lakes. The state of the system was more important in determining these patterns than seasonality, geographical location or degree of hydrological connectivity. Moreover, this strong environmental control was particularly evident in the pattern observed in one of the lakes, which shifted from a clear to a turbid state over the course of the study. This lake showed a directional selection of species from a typical clear-like to a turbid-like community. The combined DGGE/ARISA approach revealed not only broad patterns among different alternative steady states, but also more subtle differences within different regimes.

[1]  J. D. Elsas,et al.  Molecular Microbial Ecology Manual , 2013, Springer Netherlands.

[2]  I. Izaguirre,et al.  Comparison of morpho-functional phytoplankton classifications in human-impacted shallow lakes with different stable states , 2012, Hydrobiologia.

[3]  J. Comte,et al.  Composition Influences the Pathway but not the Outcome of the Metabolic Response of Bacterioplankton to Resource Shifts , 2011, PloS one.

[4]  I. Izaguirre,et al.  Picoplankton structure in clear and turbid eutrophic shallow lakes: A seasonal study , 2011 .

[5]  K. Šimek,et al.  Alga-Derived Substrates Select for Distinct Betaproteobacterial Lineages and Contribute to Niche Separation in Limnohabitans Strains , 2011, Applied and Environmental Microbiology.

[6]  F. Guillemette,et al.  Reconstructing the various facets of dissolved organic carbon bioavailability in freshwater ecosystems , 2011 .

[7]  Tamzen K. Stringham,et al.  Catastrophic Thresholds: A Synthesis of Concepts, Perspectives, and Applications , 2010 .

[8]  A. Salomon,et al.  Recruitment facilitation can drive alternative states on temperate reefs. , 2010, Ecology.

[9]  H. Grossart,et al.  Enrichment and cultivation of pelagic bacteria from a humic lake using phenol and humic matter additions. , 2010, FEMS microbiology ecology.

[10]  E. Jeppesen,et al.  Bacterioplankton in the littoral and pelagic zones of subtropical shallow lakes , 2010, Hydrobiologia.

[11]  Mary Ann Moran,et al.  Transporter genes expressed by coastal bacterioplankton in response to dissolved organic carbon , 2010, Environmental microbiology.

[12]  Horacio Zagarese,et al.  Optical characteristics of shallow lakes from the Pampa and Patagonia regions of Argentina , 2010 .

[13]  M. Demarty,et al.  In situ dissolved organic carbon (DOC) release by submerged macrophyte–epiphyte communities in southern Quebec lakes , 2009 .

[14]  S. Carpenter,et al.  Early-warning signals for critical transitions , 2009, Nature.

[15]  M. Casco,et al.  Phytoplankton and Epipelon Responses to Clear and Turbid Phases in a Seepage Lake (Buenos Aires, Argentina) , 2009 .

[16]  Horacio Zagarese,et al.  Phytoplankton and primary production in clear-vegetated, inorganic-turbid, and algal-turbid shallow lakes from the pampa plain (Argentina) , 2009, Hydrobiologia.

[17]  H. Ducklow Microbial services: challenges for microbial ecologists in a changing world , 2008 .

[18]  W. Ye,et al.  Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. , 2007, FEMS microbiology ecology.

[19]  J. Boenigk,et al.  Stuck in the mud: suspended sediments as a key issue for survival of chrysomonad flagellates , 2006 .

[20]  C. Pedrós-Alió,et al.  Marine microbial diversity: can it be determined? , 2006, Trends in microbiology.

[21]  S. Langenheder,et al.  Influence of dissolved organic matter source on lake bacterioplankton structure and function--implications for seasonal dynamics of community composition. , 2006, FEMS microbiology ecology.

[22]  H. Haario,et al.  Effect of Nutrient Loading on Bacterioplankton Community Composition in Lake Mesocosms , 2006, Microbial Ecology.

[23]  E. Lindström,et al.  External control of bacterial community structure in lakes , 2006 .

[24]  S. Payette,et al.  THE CREATION OF ALTERNATIVE STABLE STATES IN THE SOUTHERN BOREAL FOREST, QUÉBEC, CANADA , 2005 .

[25]  R. Aronson,et al.  PHASE SHIFTS, ALTERNATIVE STATES, AND THE UNPRECEDENTED CONVERGENCE OF TWO REEF SYSTEMS , 2004 .

[26]  D. Haydon,et al.  Alternative stable states in ecology , 2003 .

[27]  R. Bohacek,et al.  Novel protein kinase inhibitors: SMART drug design technology. , 2003, BioTechniques.

[28]  A. Magurran,et al.  Explaining the excess of rare species in natural species abundance distributions , 2003, Nature.

[29]  C. Criddle,et al.  Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. , 2003, BioTechniques.

[30]  Armando M. Rennella,et al.  Factores que afectan la estructura y el funcionamiento de las lagunas pampeanas , 2002 .

[31]  Wim Vyverman,et al.  Relationship between Bacterial Community Composition and Bottom-Up versus Top-Down Variables in Four Eutrophic Shallow Lakes , 2002, Applied and Environmental Microbiology.

[32]  L. Meester,et al.  Contrasting bacterioplankton community composition and seasonal dynamics in two neighbouring hypertrophic freshwater lakes. , 2001, Environmental microbiology.

[33]  S. Carpenter,et al.  Catastrophic shifts in ecosystems , 2001, Nature.

[34]  J. Johansen,et al.  Is the 16S-23S rRNA internal transcribed spacer region a good tool for use in molecular systematics and population genetics? A case study in cyanobacteria. , 2001, Molecular biology and evolution.

[35]  E. Triplett,et al.  Automated Approach for Ribosomal Intergenic Spacer Analysis of Microbial Diversity and Its Application to Freshwater Bacterial Communities , 1999, Applied and Environmental Microbiology.

[36]  Edmundo E. Drago,et al.  The environmental state of Argentinean lakes: An overview , 1999 .

[37]  Martin F. Polz,et al.  Bias in Template-to-Product Ratios in Multitemplate PCR , 1998, Applied and Environmental Microbiology.

[38]  M. Scheffer Ecology of Shallow Lakes , 1997, Population and Community Biology Series.

[39]  U. Göbel,et al.  Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. , 1997, FEMS microbiology reviews.

[40]  L. Forney,et al.  Distribution of bacterioplankton in meromictic Lake Saelenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments coding for 16S rRNA , 1997, Applied and environmental microbiology.

[41]  M. Ronaghi,et al.  Real-time DNA sequencing using detection of pyrophosphate release. , 1996, Analytical biochemistry.

[42]  S. Giovannoni,et al.  Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR , 1996, Applied and environmental microbiology.

[43]  M. Scheffer,et al.  Alternative equilibria in shallow lakes. , 1993, Trends in ecology & evolution.

[44]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[45]  O. Lind,et al.  Association of turbidity and organic carbon with bacterial abundance and cell size in a large, turbid, tropical lake , 1991 .

[46]  M. Cano Fitoperifiton de un lago somero y su relación con los estados de biequilibrio , 2009 .

[47]  M. A. Quirós Vida de las Palabras , 2006 .

[48]  G. Kowalchuk,et al.  Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. , 2004 .

[49]  E. Jeppesen,et al.  Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth , 2004, Hydrobiologia.

[50]  M. Ronaghi Pyrosequencing sheds light on DNA sequencing. , 2001, Genome research.

[51]  James R. Cole,et al.  rrndb: the Ribosomal RNA Operon Copy Number Database , 2001, Nucleic Acids Res..

[52]  L. Tranvik,et al.  Enhanced bacterial growth in response to photochemical transformation of dissolved organic matter , 1995 .

[53]  H. Kramer,et al.  Applicability of light absorbance as a measure of organic carbon in humic lake water , 1982 .

[54]  R. Wetzel Limnology: Lake and River Ecosystems , 1975 .