Genomics of sponge-associated Streptomyces spp. closely related to Streptomyces albus J1074: insights into marine adaptation and secondary metabolite biosynthesis potential

PLoS One. 2014 May 12;9(5):e96719. doi: 10.1371/journal.pone.0096719. eCollection 2014.

Abstract

A total of 74 actinomycete isolates were cultivated from two marine sponges, Geodia barretti and Phakellia ventilabrum collected at the same spot at the bottom of the Trondheim fjord (Norway). Phylogenetic analyses of sponge-associated actinomycetes based on the 16S rRNA gene sequences demonstrated the presence of species belonging to the genera Streptomyces, Nocardiopsis, Rhodococcus, Pseudonocardia and Micromonospora. Most isolates required sea water for growth, suggesting them being adapted to the marine environment. Phylogenetic analysis of Streptomyces spp. revealed two isolates that originated from different sponges and had 99.7% identity in their 16S rRNA gene sequences, indicating that they represent very closely related strains. Sequencing, annotation, and analyses of the genomes of these Streptomyces isolates demonstrated that they are sister organisms closely related to terrestrial Streptomyces albus J1074. Unlike S. albus J1074, the two sponge streptomycetes grew and differentiated faster on the medium containing sea water. Comparative genomics revealed several genes presumably responsible for partial marine adaptation of these isolates. Genome mining targeted to secondary metabolite biosynthesis gene clusters identified several of those, which were not present in S. albus J1074, and likely to have been retained from a common ancestor, or acquired from other actinomycetes. Certain genes and gene clusters were shown to be differentially acquired or lost, supporting the hypothesis of divergent evolution of the two Streptomyces species in different sponge hosts.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Micromonospora / classification
  • Micromonospora / genetics
  • Phylogeny
  • Porifera / microbiology*
  • RNA, Ribosomal, 16S / genetics
  • Streptomyces / classification
  • Streptomyces / genetics*

Substances

  • RNA, Ribosomal, 16S

Grant support

This work was supported by the Research Council of Norway. DBM, MEB and MSG were partially supported by Russian state contract 8049, RFBR grant 12-04-01105 and RAS program “Molecular and Cellular Biology”. CR acknowledges a grant by the German Federal Ministry for Education and Research (0316017A). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.