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

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.

SUBMITTER: Goffredi SK

PROVIDER: S-EPMC1855680 | biostudies-literature | 2007 Apr

REPOSITORIES: biostudies-literature

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

Goffredi Shana K SK Johnson Shannon B SB Vrijenhoek Robert C RC

Applied and environmental microbiology 20070202 7

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 adul ...[more]

PMID: 17277220

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Project description:BACKGROUND:Bone-eating Osedax worms have proved to be surprisingly diverse and widespread. Including the initial description of this genus in 2004, five species that live at depths between 25 and 3,000 m in the eastern and western Pacific and in the north Atlantic have been named to date. Here, we provide molecular and morphological evidence for 12 additional evolutionary lineages from Monterey Bay, California. To assess their phylogenetic relationships and possible status as new undescribed species, we examined DNA sequences from two mitochondrial (COI and 16S rRNA) and three nuclear genes (H3, 18S and 28S rRNA). RESULTS:Phylogenetic analyses identified 17 distinct evolutionary lineages. Levels of sequence divergence among the undescribed lineages were similar to those found among the named species. The 17 lineages clustered into five well-supported clades that also differed for a number of key morphological traits. Attempts to determine the evolutionary age of Osedax depended on prior assumptions about nucleotide substitution rates. According to one scenario involving a molecular clock calibrated for shallow marine invertebrates, Osedax split from its siboglinid relatives about 45 million years ago when archeocete cetaceans first appeared and then diversified during the late Oligocene and early Miocene when toothed and baleen whales appeared. Alternatively, the use of a slower clock calibrated for deep-sea annelids suggested that Osedax split from its siboglinid relatives during the Cretaceous and began to diversify during the Early Paleocene, at least 20 million years before the origin of large marine mammals. CONCLUSION:To help resolve uncertainties about the evolutionary age of Osedax, we suggest that the fossilized bones from Cretaceous marine reptiles and late Oligocene cetaceans be examined for possible trace fossils left by Osedax roots. Regardless of the outcome, the present molecular evidence for strong phylogenetic concordance across five separate genes suggests that the undescribed Osedax lineages comprise evolutionarily significant units that have been separate from one another for many millions of years. These data coupled with ongoing morphological analyses provide a solid foundation for their future descriptions as new species.

Project description:Osedax, the deep-sea annelid found at sunken whalefalls, is known to host Oceanospirillales bacterial endosymbionts intracellularly in specialized roots, which help it feed exclusively on vertebrate bones. Past studies, however, have also made mention of external bacteria on their trunks. During a 14-yr study, we reveal a dynamic, yet persistent, shift of Campylobacterales integrated into the epidermis of Osedax, which change over time as the whale carcass degrades on the sea floor. The Campylobacterales associated with seven species of Osedax, which comprise 67% of the bacterial community on the trunk, appear initially dominated by the genus Arcobacter (at early time points <24 mo), the Sulfurospirillum at intermediate stages (~50 mo), and the Sulfurimonas at later stages (>140 mo) of whale carcass decomposition. Metagenome analysis of the epibiont metabolic capabilities suggests potential for a transition from heterotrophy to autotrophy and differences in their capacity to metabolize oxygen, carbon, nitrogen, and sulfur. Compared to free-living relatives, the Osedax epibiont genomes were enriched in transposable elements, implicating genetic exchange on the host surface, and contained numerous secretions systems with eukaryotic-like protein (ELP) domains, suggesting a long evolutionary history with these enigmatic, yet widely distributed deep-sea worms. IMPORTANCE Symbiotic associations are widespread in nature and we can expect to find them in every type of ecological niche. In the last twenty years, the myriad of functions, interactions and species comprising microbe-host associations has fueled a surge of interest and appreciation for symbiosis. During this 14-year study, we reveal a dynamic population of bacterial epibionts, integrated into the epidermis of 7 species of a deep-sea worm group that feeds exclusively on the remains of marine mammals. The bacterial genomes provide clues of a long evolutionary history with these enigmatic worms. On the host surface, they exchange genes and appear to undergo ecological succession, as the whale carcass habitat degrades over time, similar to what is observed for some free-living communities. These, and other annelid worms are important keystone species for diverse deep-sea environments, yet the role of attached external bacteria in supporting host health has received relatively little attention.

Dataset Information

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

Publications

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

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