Original Article

Subject Category: Microbial population and community ecology

The ISME Journal (2010) 4, 739–751; doi:10.1038/ismej.2010.1; published online 11 February 2010

Viral and microbial community dynamics in four aquatic environments

Beltran Rodriguez-Brito1,2,9, LinLin Li2,9,10, Linda Wegley2, Mike Furlan2, Florent Angly1,2, Mya Breitbart2,11, John Buchanan3, Christelle Desnues2,12, Elizabeth Dinsdale2, Robert Edwards1,2, Ben Felts4, Matthew Haynes2, Hong Liu2, David Lipson2, Joseph Mahaffy4, Anna Belen Martin-Cuadrado5, Alex Mira5,13, Jim Nulton4, Lejla Pašić5,6, Steve Rayhawk1,2, Jennifer Rodriguez-Mueller2, Francisco Rodriguez-Valera5, Peter Salamon4, Shailaja Srinagesh2, Tron Frede Thingstad8, Tuong Tran2, Rebecca Vega Thurber2,14, Dana Willner2, Merry Youle7 and Forest Rohwer2

  1. 1Computational Science Research Center, San Diego State University, San Diego, CA, USA
  2. 2Department of Biology, San Diego State University, San Diego, CA, USA
  3. 3Aqua Bounty Technologies, San Diego, CA, USA
  4. 4Department of Mathematics, San Diego State University, San Diego, CA, USA
  5. 5Evolutionary Genomics Group, División de Microbiología, Universidad Miguel Hernández, San Juan de Alicante, Spain
  6. 6Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia
  7. 7Rainbow Rock, Ocean View, HI, USA
  8. 8Department of Biology, University of Bergen, Bergen, Norway

Correspondence: B Rodriguez-Brito, Computational Science Research Center, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182-1245, USA. E-mail: beltran.rodriguezbrito@gmail.com

9These authors contributed equally to this work.

10Current address: Delwart Lab, Blood System Research Institute, San Francisco, CA, USA.

11Current address: College of Marine Science, University of South Florida, FL, USA.

12Current address: URMITE, UMR CNRS-IRD 6236, Universite de la Mediterranee, Marseille, France.

13Current address: Center for Advanced Research in Public Health, CSISP, Area de Genomica y Salud, Valencia, Spain.

14Current address: Biology Department, Florida International University, Miami, Florida, USA.

Received 15 September 2009; Revised 22 December 2009; Accepted 23 December 2009; Published online 11 February 2010.

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Abstract

The species composition and metabolic potential of microbial and viral communities are predictable and stable for most ecosystems. This apparent stability contradicts theoretical models as well as the viral–microbial dynamics observed in simple ecosystems, both of which show Kill-the-Winner behavior causing cycling of the dominant taxa. Microbial and viral metagenomes were obtained from four human-controlled aquatic environments at various time points separated by one day to >1 year. These environments were maintained within narrow geochemical bounds and had characteristic species composition and metabolic potentials at all time points. However, underlying this stability were rapid changes at the fine-grained level of viral genotypes and microbial strains. These results suggest a model wherein functionally redundant microbial and viral taxa are cycling at the level of viral genotypes and virus-sensitive microbial strains. Microbial taxa, viral taxa, and metabolic function persist over time in stable ecosystems and both communities fluctuate in a Kill-the-Winner manner at the level of viral genotypes and microbial strains.

Keywords:

viruses; community dynamics; Kill-the-Winner; metagenomics; aquatic environments

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