Genetic Diversity and Potential Function of Microbial Symbionts Associated with Newly Discovered Species of Osedax Polychaete Worms

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

A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida)

<p>Abstract</p> <p>Background</p> <p>Bone-eating <it>Osedax </it>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 (<it>COI </it>and <it>16S </it>rRNA) and three nuclear genes (<it>H3</it>, <it>18S </it>and <it>28S </it>rRNA).</p> <p>Results</p> <p>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 <it>Osedax </it>depended on prior assumptions about nucleotide substitution rates. According to one scenario involving a molecular clock calibrated for shallow marine invertebrates, <it>Osedax </it>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 <it>Osedax </it>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.</p> <p>Conclusion</p> <p>To help resolve uncertainties about the evolutionary age of <it>Osedax</it>, we suggest that the fossilized bones from Cretaceous marine reptiles and late Oligocene cetaceans be examined for possible trace fossils left by <it>Osedax </it>roots. Regardless of the outcome, the present molecular evidence for strong phylogenetic concordance across five separate genes suggests that the undescribed <it>Osedax </it>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.</p

Population structure and connectivity in Indo-Pacific deep-sea mussels of the Bathymodiolus septemdierum complex

Current pressures to mine polymetallic sulfide deposits pose threats to the animal communities found at deep-sea hydrothermal vents. Management plans aimed at preserving these unusual communities require knowledge of historical and contemporary forces that shaped the distributions and connectivity of associated species. As most vent research has focused on the eastern Pacific and mid-Atlantic ridge systems less is known about Indo-Pacific vents, where mineral extraction activities are imminent. Deep-sea mussels (Bivalvia: Mytilidae) of the genus Bathymodiolus include the morphotypic species B. septemdierum, B. brevior, B. marisindicus, and B. elongatus which are among the dominant vent taxa in western Pacific back-arc basins and the Central Indian Ridge. To assess their interpopulational relationships, we examined multilocus genotypes based on DNA sequences from four nuclear and four mitochondrial genes, and allozyme variation encoded by eleven genes. Bayesian assignment methods grouped mussels from seven widespread western Pacific localities into a single cluster, whereas the Indian Ocean mussels were clearly divergent. Thus, we designate two regional metapopulations. Notably, contemporary migration rates among all sites appeared to be low despite limited population differentiation, which highlights the necessity of obtaining realistic data on recovery times and fine-scale population structure to develop and manage conservation units effectively. Future studies using population genomic methods to address these issues in a range of species will help to inform management plans aimed at mitigating potential impacts of deep-sea mining in the Indo-Pacific region

Allopatric and Sympatric Drivers of Speciation in Alviniconcha Hydrothermal Vent Snails

Despite significant advances in our understanding of speciation in the marine environment, the mechanisms underlying evolutionary diversification in deep-sea habitats remain poorly investigated. Here, we used multigene molecular clocks and population genetic inferences to examine processes that led to the emergence of the six extant lineages of Alviniconcha snails, a key taxon inhabiting deep-sea hydrothermal vents in the Indo-Pacific Ocean. We show that both allopatric divergence through historical vicariance and ecological isolation due to niche segregation contributed to speciation in this genus. The split between the two major Alviniconcha clades (separating A. boucheti and A. marisindica from A. kojimai, A. hessleri, and A. strummeri) probably resulted from tectonic processes leading to geographic separation, whereas the splits between co-occurring species might have been influenced by ecological factors, such as the availability of specific chemosynthetic symbionts. Phylogenetic origin of the sixth species, Alviniconcha adamantis, remains uncertain, although its sister position to other extant Alviniconcha lineages indicates a possible ancestral relationship. This study lays a foundation for future genomic studies aimed at deciphering the roles of local adaptation, reproductive biology, and host–symbiont compatibility in speciation of these vent-restricted snails

Genetic Variation Among Endosymbionts of Widely Distributed Vestimentiferan Tubeworms

Vestimentiferan tubeworms thriving in sulfidic deep-sea hydrothermal vents and cold seeps are constrained by their nutritional reliance on chemoautotrophic endosymbionts. In a recent phylogenetic study using 16S ribosomal DNA, we found that endosymbionts from vent and seep habitats form two distinct clades,vith little variation within each clade. In the present study, we used two different approaches to assess the genetic variation among biogeographically distinct vestimentiferan symbionts, DNA sequences were obtained for the noncoding, internal transcribed spacer (ITS) regions of the rRNA operons of symbionts associated with six different genera of vestimentiferan tubeworms. ITS sequences from endosymbionts of host genera collected from different habitats and widely distributed vent sites were surprisingly conserved. Because the ITS region was not sufficient for distinguishing endosymbionts from different habitats or locations, we used a DNA fingerprinting technique, repetitive extragenic-palindrome PCR (REP-PCR), to reveal differences in the distribution of repetitive sequences in the genomes of the bacterial endosymbionts. Most of the endosymbionts displayed unique REP-PCR patterns. A cladogram generated from these fingerprints reflected relationships that may be influenced by a variety of factors, including host genera, geographic location, and bottom type

Host hybridization as a potential mechanism of lateral symbiont transfer in deep‐sea vesicomyid clams

Deep‐sea vesicomyid clams live in mutualistic symbiosis with chemosynthetic bacteria that are inherited through the maternal germ line. On evolutionary timescales, strictly vertical transmission should lead to cospeciation of host mitochondrial and symbiont lineages; nonetheless, examples of incongruent phylogenies have been reported, suggesting that symbionts are occasionally horizontally transmitted between host species. The current paradigm for vesicomyid clams holds that direct transfers cause host shifts or mixtures of symbionts. An alternative hypothesis suggests that hybridization between host species might explain symbiont transfers. Two clam species, Archivesica gigas and Phreagena soyoae, frequently co‐occur at deep‐sea hydrocarbon seeps in the eastern Pacific Ocean. Although the two species typically host gammaproteobacterial symbiont lineages marked by divergent 16S rRNA phylotypes, we identified a number of clams with the A. gigas mitotype that hosted symbionts with the P. soyoae phylotype. Demographic inference models based on genome‐wide SNP data and three Sanger sequenced gene markers provided evidence that A. gigas and P. soyoae hybridized in the past, supporting the hypothesis that hybridization might be a viable mechanism of interspecific symbiont transfer. These findings provide new perspectives on the evolution of vertically transmitted symbionts and their hosts in deep‐sea chemosynthetic environments

The spatial scale of genetic subdivision in populations of Ifremeria nautilei, a hydrothermal-vent gastropod from the southwest Pacific

<p>Abstract</p> <p>Background</p> <p>Deep-sea hydrothermal vents provide patchy, ephemeral habitats for specialized communities of animals that depend on chemoautotrophic primary production. Unlike eastern Pacific hydrothermal vents, where population structure has been studied at large (thousands of kilometres) and small (hundreds of meters) spatial scales, population structure of western Pacific vents has received limited attention. This study addresses the scale at which genetic differentiation occurs among populations of a western Pacific vent-restricted gastropod, <it>Ifremeria nautilei</it>.</p> <p>Results</p> <p>We used mitochondrial and DNA microsatellite markers to infer patterns of gene flow and population subdivision. A nested sampling strategy was employed to compare genetic diversity in discrete patches of <it>Ifremeria nautilei </it>separated by a few meters within a single vent field to distances as great as several thousand kilometres between back-arc basins that encompass the known range of the species. No genetic subdivisions were detected among patches, mounds, or sites within Manus Basin. Although <it>I. nautilei </it>from Lau and North Fiji Basins (~1000 km apart) also exhibited no evidence for genetic subdivision, these populations were genetically distinct from the Manus Basin population.</p> <p>Conclusions</p> <p>An unknown process that restricts contemporary gene flow isolates the Manus Basin population of <it>Ifremeria nautilei </it>from widespread populations that occupy the North Fiji and Lau Basins. A robust understanding of the genetic structure of hydrothermal vent populations at multiple spatial scales defines natural conservation units and can help minimize loss of genetic diversity in situations where human activities are proposed and managed.</p

Feeding behavior in sexual and clonal strains of Poeciliopsis

Sexual and clonal fish of the genus Poeciliopsis occur together in desert streams of Sonora, Mexico. Their coexistence has been explained in terms of niche partitioning for food and space. We examined predatory behavior that might influence niche relationships, and found significant differences among two coexisting sperm-dependent clonal strains and their two sexual progenitors. Handling time and prey manipulation of free-swimming ( Artemia ) and benthic (chironomid larvae) prey differed significantly among sexual and clonal strains. Analyses of gut contents from field-collected fish revealed that the laboratory estimates of predatory efficiency were related to their feeding behavior in nature. Behavior differences, such as those described herein, contribute to our understanding of the mechanisms of unisexual/bisexual coexistence in Poeciliopsis .Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/46898/1/265_2004_Article_BF00168589.pd

Genetic diversity and demographic instability in Riftia pachyptila tubeworms from eastern Pacific hydrothermal vents

<p>Abstract</p> <p>Background</p> <p>Deep-sea hydrothermal vent animals occupy patchy and ephemeral habitats supported by chemosynthetic primary production. Volcanic and tectonic activities controlling the turnover of these habitats contribute to demographic instability that erodes genetic variation within and among colonies of these animals. We examined DNA sequences from one mitochondrial and three nuclear gene loci to assess genetic diversity in the siboglinid tubeworm, <it>Riftia pachyptila</it>, a widely distributed constituent of vents along the East Pacific Rise and Galápagos Rift.</p> <p>Results</p> <p>Genetic differentiation (<it>F</it>_<it>ST</it>) among populations increased with geographical distances, as expected under a linear stepping-stone model of dispersal. Low levels of DNA sequence diversity occurred at all four loci, allowing us to exclude the hypothesis that an idiosyncratic selective sweep eliminated mitochondrial diversity alone. Total gene diversity declined with tectonic spreading rates. The southernmost populations, which are subjected to superfast spreading rates and high probabilities of extinction, are relatively homogenous genetically.</p> <p>Conclusions</p> <p>Compared to other vent species, DNA sequence diversity is extremely low in <it>R. pachyptila</it>. Though its dispersal abilities appear to be effective, the low diversity, particularly in southern hemisphere populations, is consistent with frequent local extinction and (re)colonization events.</p