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Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms - PubMed

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Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms

Shana K Goffredi et al. Appl Environ Microbiol. 2007 Apr.

Abstract

We investigated the genetic diversity of symbiotic bacteria associated with two newly discovered species of Osedax from Monterey Canyon, CA, at 1,017-m (Osedax Monterey Bay sp. 3 "rosy" [Osedax sp. MB3]) and 381-m (Osedax Monterey Bay sp. 4 "yellow collar") depths. Quantitative PCR and clone libraries of 16S rRNA gene sequences identified differences in the compositions and abundances of bacterial phylotypes associated with the newly discovered host species and permitted comparisons between adult Osedax frankpressi and juveniles that had recently colonized whalebones implanted at 2,891 m. The newly discovered Osedax species hosted Oceanospirillales symbionts that are related to Gammaproteobacteria associated with the previously described O. frankpressi and Osedax rubiplumus (S. K. Goffredi, V. J. Orphan, G. W. Rouse, L. Jahnke, T. Embaye, K. Turk, R. Lee, and R. C. Vrijenhoek, Environ. Microbiol. 7:1369-1378, 2005). In addition, Osedax sp. MB3 hosts a diverse and abundant population of additional bacteria dominated by Epsilonproteobacteria. Ultrastructural analysis of symbiont-bearing root tissues verified the enhanced microbial diversity of Osedax sp. MB3. Root tissues from the newly described host species and O. frankpressi all exhibited collagenolytic enzyme activity, which covaried positively with the abundance of symbiont DNA and negatively with mean adult size of the host species. Members of this unusual genus of bone-eating worms may form variable associations with symbiotic bacteria that allow for the observed differences in colonization and success in whale fall environments throughout the world's oceans.

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Figures

FIG. 1.
FIG. 1.

Osedax spp. (A) Adult O. frankpressi. (B) Osedax sp. MB3 (“rosy”). (C) Osedax sp. MB4 (“yellow collar”). (D) Juvenile O. frankpressi recruited to implanted whalebones. (E) Implanted whalebones (partial jawbone of a blue whale). All bars are 1 mm, except in E (bar, 70 cm).

FIG. 2.
FIG. 2.

Phylogenetic relationships, based on 16S rRNA, between free-living members of the Oceanospirillales (Gammaproteobacteria) and the symbiont ribotypes associated with Osedax worms (boldfaced taxa designated by dive.individual.clone) (Table 2). The number following the dive represents an individual worm, and the following letter/number is a unique 16S sequence from clone libraries. GenBank accession numbers for sequences acquired during this study are DQ911529 to DQ911547. The maximum likelihood tree was generated from sequences treated with the GTR+I+G model. Arrows at nodes indicate support for the internal clade (phylotypes P1 to P6) designations. The numbers at the nodes represent bootstrap values (maximum likelihood)/posterior probability values (Bayesian).

FIG. 3.
FIG. 3.

Phylogenetic relationships, based on 16S rRNA, between free-living members of the Epsilonproteobacteria and bacterial ribotypes associated with Osedax sp. MB3 (boldfaced taxa designated by dive.individual.clone) (Table 2). The number following the dive represents an individual worm, and the following letter/number is a unique 16S sequence from clone libraries. GenBank accession numbers for sequences acquired during this study are EF100881 to EF100889. The numbers at the nodes represent bootstrap values (neighbor joining/parsimony).

FIG. 4.
FIG. 4.

Osedax species symbionts. Images of FISH microscopy of the primary symbiont within the roots of Osedax sp. MB3 (A and D), Osedax sp. MB4 (B and E), and juvenile recruits of O. frankpressi (C and F) are shown. A to F are hybridizations with the symbiont-specific sym435 probe labeled with Cy3 (shown in red). C and F are dual stained with a eukaryote-specific Cy5-labeled probe (shown in green). All images are embedded sections (7 to 20 μm thick) that were also stained with DAPI prior to imaging (shown in blue, except in D). Images were captured with softWoRx 3.4.4 (Applied Precision). Intact bacteriocytes (arrowheads) and the external surface of root tissue (arrows) are shown. s, symbiont. All bars are 50 μm, except in E (bar, 10 μm).

FIG. 5.
FIG. 5.

Additional bacteria associated with Osedax sp. MB3. All are hybridizations with a general bacterial EUB338 probe labeled with Cy3 (shown in red). Bars, 50 μm (A) and 10 μm (B to D). m, mucous layer; b, bacteria.

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