Original Article

Subject Category: Integrated genomics and post-genomics approaches in microbial ecology

The ISME Journal (2009) 3, 1193–1203; doi:10.1038/ismej.2009.58; published online 28 May 2009

Genomic islands link secondary metabolism to functional adaptation in marine Actinobacteria

Kevin Penn1, Caroline Jenkins1, Markus Nett1, Daniel W Udwary1, Erin A Gontang1, Ryan P McGlinchey1, Brian Foster2, Alla Lapidus2, Sheila Podell1, Eric E Allen1, Bradley S Moore1,3 and Paul R Jensen1

  1. 1Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA, USA
  2. 2Department of Energy, Joint Genome Institute-Lawrence Berkeley National Laboratory, Walnut Creek, CA, USA
  3. 3Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California San Diego, La Jolla, CA, USA

Correspondence: PR Jensen, Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093, USA. E-mail: pjensen@ucsd.edu; BS Moore, Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093, USA. E-mail: bsmoore@ucsd.edu

Received 9 February 2009; Revised 9 April 2009; Accepted 21 April 2009; Published online 28 May 2009.

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Abstract

Genomic islands have been shown to harbor functional traits that differentiate ecologically distinct populations of environmental bacteria. A comparative analysis of the complete genome sequences of the marine Actinobacteria Salinispora tropica and Salinispora arenicola reveals that 75% of the species-specific genes are located in 21 genomic islands. These islands are enriched in genes associated with secondary metabolite biosynthesis providing evidence that secondary metabolism is linked to functional adaptation. Secondary metabolism accounts for 8.8% and 10.9% of the genes in the S. tropica and S. arenicola genomes, respectively, and represents the major functional category of annotated genes that differentiates the two species. Genomic islands harbor all 25 of the species-specific biosynthetic pathways, the majority of which occur in S. arenicola and may contribute to the cosmopolitan distribution of this species. Genome evolution is dominated by gene duplication and acquisition, which in the case of secondary metabolism provide immediate opportunities for the production of new bioactive products. Evidence that secondary metabolic pathways are exchanged horizontally, coupled with earlier evidence for fixation among globally distributed populations, supports a functional role and suggests that the acquisition of natural product biosynthetic gene clusters represents a previously unrecognized force driving bacterial diversification. Species-specific differences observed in clustered regularly interspaced short palindromic repeat sequences suggest that S. arenicola may possess a higher level of phage immunity, whereas a highly duplicated family of polymorphic membrane proteins provides evidence for a new mechanism of marine adaptation in Gram-positive bacteria.

Keywords:

comparative genomics, genomic islands, marine Actinobacteria, Salinispora, secondary metabolites

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