Original Article

Subject Category: Microbial ecology and functional diversity of natural habitats

The ISME Journal (2009) 3, 1286–1300; doi:10.1038/ismej.2009.75; published online 2 July 2009

Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean

Ian Hewson1, Rachel S Poretsky2, Sonya T Dyhrman3, Brian Zielinski4, Angelicque E White5, H James Tripp1, Joseph P Montoya6 and Jonathan P Zehr1

  1. 1Department of Ocean Sciences, University of California Santa Cruz, Santa Cruz, CA, USA
  2. 2Department of Marine Science, University of Georgia, Athens, GA, USA
  3. 3Biology Department, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
  4. 4Department of Marine Science, University of South Florida, St Petersburg, FL, USA
  5. 5College of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis, OR, USA
  6. 6School of Biology, Georgia Institute of Technology, Atlanta, GA, USA

Correspondence: I Hewson, Department of Microbiology, Cornell University, Wing Hall 403, Ithaca, NY 14853, USA. E-mail: hewson@cornell.edu

Received 30 March 2009; Revised 26 May 2009; Accepted 30 May 2009; Published online 2 July 2009.

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Abstract

Trichodesmium are responsible for a large fraction of open ocean nitrogen fixation, and are often found in complex consortia of other microorganisms, including viruses, prokaryotes, microbial eukaryotes and metazoa. We applied a community gene expression (metatranscriptomic) approach to study the patterns of microbial gene utilization within colonies of Trichodesmium collected during a bloom in the Southwest Pacific Ocean in April 2007. The survey generated 5711-day and 5385-night putative mRNA reads. The majority of mRNAs were from the co-occurring microorganisms and not Trichodesmium, including other cyanobacteria, heterotrophic bacteria, eukaryotes and phage. Most transcripts did not share homology with proteins from cultivated microorganisms, but were similar to shotgun sequences and unannotated proteins from open ocean metagenomic surveys. Trichodesmium transcripts were mostly expressed photosynthesis, N2 fixation and S-metabolism genes, whereas those in the co-occurring microorganisms were mostly involved in genetic information storage and processing. Detection of Trichodesmium genes involved in P uptake and As detoxification suggest that local enrichment of N through N2 fixation may lead to a P-stress response. Although containing similar dominant transcripts to open ocean metatranscriptomes, the overall pattern of gene expression in Trichodesmium colonies was distinct from free-living pelagic assemblages. The identifiable genes expressed by Trichodesmium and closely associated microorganisms reflect the constraints of life in well-lit and nutrient-poor waters, with biosynthetic investment in nutrient acquisition and cell maintenance, which is in contrast to gene transcription by soil and coastal seawater microbial assemblages. The results provide insight into aggregate microbial communities in contrast to planktonic free-living assemblages that are the focus of other studies.

Keywords:

Trichdoesmium, metatranscriptomics, aggregate, gene expression, community

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