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

Elena Ian et al. PLoS One. 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.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1

Figure 1. 16S rRNA gene-based neighbor-joining phylogenetic tree of Streptomyces spp. isolated from Phakellia ventilabrum and Geodia barretti with bootstrap values (1000 replications).

The nearest neighbors revealed through BLAST search of non-redundant nucleotide sequences in the public databases are presented in the tree. Nucleotide sequence accession numbers are given in brackets. The scale bar corresponds to 0.02 substitutions per nucleotide positions. Isolates chosen for further analysis are marked with a dotted box.

Figure 2

Figure 2. Comparison of growth and differentiation of Streptomyces spp. PVA 94-07 and GBA 94-10, and S. albus J1074 on ISP2 agar medium with (A) and without (B) sea water.

Figure 3

Figure 3. Orthologs row-based comparison of genome content of Streptomyces spp. PVA 94-07, GBA 94-10, S. albus J1074, and 11 other Streptomyces spp. shown as a Venn diagram.

Numbers of co-orthologs are given in parentheses.

Figure 4

Figure 4. Venn diagram showing unique genes found in the genomes of PVA-94-07, GBA 94-10 and S. albus J1074, and some marine bacteria, but not in other Streptomyces investigated.

Paralogs (OrthoMCL co-orthologs) are shown in parentheses.

Figure 5

Figure 5. Enterocin biosynthesis gene clusters identified in the genomes of Streptomyces spp. PVA 94-07 and GBA 94-10.

Genomic region of S. albus J1074 where the cluster has been inserted is shown in the middle.

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