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BACKGROUND: Numerous deep-sea invertebrates, at both hydrothermal vents and methane seeps, have formed symbiotic associations with internal chemosynthetic bacteria in order to harness inorganic energy sources typically unavailable to animals. Despite success in nearly all marine habitats and their well-known associations with photosynthetic symbionts, Cnidaria remain one of the only phyla present in the deep-sea without a clearly documented example of dependence on chemosynthetic symbionts. RESULTS: A new chemosynthetic symbiosis between the sea anemone Ostiactis pearseae and intracellular bacteria was discovered at ~ 3700 m deep hydrothermal vents in the southern Pescadero Basin, Gulf of California. Unlike most sea anemones observed from chemically reduced habitats, this species was observed in and amongst vigorously venting fluids, side-by-side with the chemosynthetic tubeworm Oasisia aff. alvinae. Individuals of O. pearseae displayed carbon, nitrogen, and sulfur tissue isotope values suggestive of a nutritional strategy distinct from the suspension feeding or prey capture conventionally employed by sea anemones. Molecular and microscopic evidence confirmed the presence of intracellular SUP05-related bacteria housed in the tentacle epidermis of O. pearseae specimens collected from 5 hydrothermally active structures within two vent fields ~ 2 km apart. SUP05 bacteria (Thioglobaceae) dominated the O. pearseae bacterial community, but were not recovered from other nearby anemones, and were generally rare in the surrounding water. Further, the specific Ostiactis-associated SUP05 phylotypes were not detected in the environment, indicating a specific association. Two unusual candidate bacterial phyla (the OD1 and BD1-5 groups) appear to associate exclusively with O. pearseae and may play a role in symbiont sulfur cycling. CONCLUSION: The Cnidarian Ostiactis pearseae maintains a physical and nutritional alliance with chemosynthetic bacteria. The mixotrophic nature of this symbiosis is consistent with what is known about other cnidarians and the SUP05 bacterial group, in that they both form dynamic relationships to succeed in nature. The advantages gained by appropriating metabolic and structural resources from each other presumably contribute to their striking abundance in the Pescadero Basin, at the deepest known hydrothermal vents in the Pacific Ocean.

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BACKGROUND: Darwin's finches are a clade of 19 species of passerine birds native to the Galápagos Islands, whose biogeography, specialized beak morphologies, and dietary choices-ranging from seeds to blood-make them a classic example of adaptive radiation. While these iconic birds have been intensely studied, the composition of their gut microbiome and the factors influencing it, including host species, diet, and biogeography, has not yet been explored. RESULTS: We characterized the microbial community associated with 12 species of Darwin's finches using high-throughput 16S rRNA sequencing of fecal samples from 114 individuals across nine islands, including the unusual blood-feeding vampire finch (Geospiza septentrionalis) from Darwin and Wolf Islands. The phylum-level core gut microbiome for Darwin's finches included the Firmicutes, Gammaproteobacteria, and Actinobacteria, with members of the Bacteroidetes at conspicuously low abundance. The gut microbiome was surprisingly well conserved across the diversity of finch species, with one exception-the vampire finch-which harbored bacteria that were either absent or extremely rare in other finches, including Fusobacterium, Cetobacterium, Ureaplasma, Mucispirillum, Campylobacter, and various members of the Clostridia-bacteria known from the guts of carnivorous birds and reptiles. Complementary stable isotope analysis of feathers revealed exceptionally high δ15N isotope values in the vampire finch, resembling top marine predators. The Galápagos archipelago is also known for extreme wet and dry seasons, and we observed a significant seasonal shift in the gut microbial community of five additional finch species sampled during both seasons. CONCLUSIONS: This study demonstrates the overall conservatism of the finch gut microbiome over short (< 1 Ma) divergence timescales, except in the most extreme case of dietary specialization, and elevates the evolutionary importance of seasonal shifts in driving not only species adaptation, but also gut microbiome composition.

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Betaproteobacteria were the most common isolates from the water-filled tank of a Costa Rican bromeliad. Isolates included eight species from the orders Neisseriales and Burkholderiales, with close relatives recovered previously from tropical soils, wetlands, freshwater, or in association with plants. Compared to close relatives, the isolates displayed high temperature and comparatively low pH optima, reflecting the tropical, acidic nature of the bromeliad tank. Bromeliad-associated bacteria most closely related to Chromobacterium, Herbaspirillum, and Aquitalea were all isolated exclusively at pH 6, while Ralstonia, Cupriavidus, and three species of Burkholderia were isolated mostly at pH 4. Activity profiles for the isolates suggest pervasive capabilities for the breakdown of plant-sourced organics, including d-galacturonic acid, mannitol, d-xylose, and l-phenylalanine, also reflecting a niche dominated by decomposition of leaves from the overlying canopy, which become entrained in the tanks. Metabolic activity profiles were overlapping between the Burkholderiales, isolated at pH 4, and the Neisseriales, isolated at pH 6, suggesting that plant material decomposition, which is presumably the underlying process sustaining the tank community and possibly the plant itself, occurs in the tanks at both pH extremes. These results suggest that bromeliad-associated betaproteobacteria may play an important role in the cycling of carbon in this unusual aquatic habitat.

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Interdomain symbioses with bacteria allow insects to take advantage of underutilized niches and provide the foundation for their evolutionary success in neotropical ecosystems. The gut microbiota of 13 micro-allopatric tropical pentatomid species, from a Costa Rican lowland rainforest, was characterized and compared with insect and host plant phylogenies. Like other families within the Pentatomomorpha, these insects (within seven genera-Antiteuchus, Arvelius, Edessa, Euschistus, Loxa, Mormidea, and Sibaria) house near-monocultures of gamma-proteobacteria in midgut crypts, comprising three distinct lineages within the family Enterobacteriaceae. Identity of the dominant bacteria (78-100% of the recovered 16S rRNA genes) was partially congruent with insect phylogeny, at the level of subfamily and tribe, with bacteria closely related to Erwinia observed in six species of the subfamily Pentatominae, and bacteria in a novel clade of Enterobacteriaceae for seven species within the subfamilies Edessinae and Discocephalinae. Symbiont replacement (i.e., bacterial "contamination" from the environment) may occur during maternal transmission by smearing of bacteria onto the egg surfaces during oviposition. This transmission strategy was experimentally confirmed for Sibaria englemani, and suspected for four species from two subfamilies, based on observation of egg probing by nymphs. Symbiont-deprived S. englemani, acquired via egg surface sterilization, exhibited significantly extended second instars (9.1 days compared with 7.9 days for symbiotic nymphs; p = 0.0001, Wilcoxon's rank with Bonferroni correction), slower linearized growth rates (p = 0.005, Welch 2-sample t-test), and qualitative differences in ceca morphology, including increased translucency of crypts, elongation of extracellular cavities, and distribution of symbionts, compared to symbiotic nymphs. Combined, these results suggest a role of the symbiont in host development, the reliable transference of symbionts via egg surfaces, and a suggestion of co-evolution between symbiont and tropical pentatomid host insects.

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Recent investigations have demonstrated that unusually 'hairy' yeti crabs within the family Kiwaidae associate with two predominant filamentous bacterial families, the Epsilon and Gammaproteobacteria. These analyses, however, were based on samples collected from a single body region, the setae of pereopods. To more thoroughly investigate the microbiome associated with Kiwa puravida, a yeti crab species from Costa Rica, we utilized barcoded 16S rRNA amplicon pyrosequencing, as well as microscopy and terminal restriction fragment length polymorphism analysis. Results indicate that, indeed, the bacterial community on the pereopods is far less diverse than on the rest of the body (Shannon indices ranged from 1.30-2.02 and 2.22-2.66, respectively). Similarly, the bacterial communities associated with juveniles and adults were more complex than previously recognized, with as many as 46 bacterial families represented. Ontogenetic differences in the microbial community, from egg to juvenile to adult, included a dramatic under-representation of the Helicobacteraceae and higher abundances of both Thiotrichaceae and Methylococcaceae for the eggs, which paralleled patterns observed in another bacteria-crustacean symbiosis. The degree to which abiotic and biotic feedbacks influence the bacterial community on the crabs is still not known, but predictions suggest that both the local environment and host-derived factors influence the establishment and maintenance of microbes associated with the surfaces of aquatic animals.

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Upon their initial discovery, hydrothermal vents and methane seeps were considered to be related but distinct ecosystems, with different distributions, geomorphology, temperatures, geochemical properties and mostly different species. However, subsequently discovered vents and seep systems have blurred this distinction. Here, we report on a composite, hydrothermal seep ecosystem at a subducting seamount on the convergent Costa Rica margin that represents an intermediate between vent and seep ecosystems. Diffuse flow of shimmering, warm fluids with high methane concentrations supports a mixture of microbes, animal species, assemblages and trophic pathways with vent and seep affinities. Their coexistence reinforces the continuity of reducing environments and exemplifies a setting conducive to interactive evolution of vent and seep biota.

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Tank-forming bromeliads, suspended in the rainforest canopy, possess foliage arranged in compact rosettes capable of long-term retention of rainwater. This large and unique aquatic habitat is inhabited by microorganisms involved in the important decomposition of impounded material. Moreover, these communities are likely influenced by environmental factors such as pH, oxygen, and light. Bacterial community composition and diversity was determined for the tanks of several bromeliad species (Aechmea and Werauhia) from northern Costa Rica, which span a range of parameters, including tank morphology and pH. These were compared with a nearby forest soil sample, an artificial tank (amber bottle), and a commercially available species (Aechmea). Bacterial community diversity, as measured by 16S rRNA analysis and tRFLP, showed a significant positive correlation with tank pH. A majority of 16S rRNA bacterial phylotypes found in association with acidic bromeliad tanks of pH < 5.1 were affiliated with the Alphaproteobacteria, Acidobacteria, Planctomycetes, and Bacteroidetes, and were similar to those found in acidic peat bogs, yet distinct from the underlying soil community. In contrast, bromeliads with tank pH > 5.3, including the commercial bromeliad with the highest pH (6.7), were dominated by Betaproteobacteria, Firmicutes, and Bacteroidetes. To empirically determine the effect of pH on bacterial community, the tank pH of a specimen of Aechmea was depressed, in the field, from 6.5 to 4.5, for 62 days. The resulting community changed predictably with decreased abundance of Betaproteobacteria and Firmicutes and a concomitant increase in Alphaproteobacteria and Acidobacteria. Collectively, these results suggest that bromeliad tanks provide important habitats for a diverse microbial community, distinct from the surrounding environment, which are influenced greatly by acid-base conditions. Additionally, total organic carbon (∼46%) and nitrogen (∼2%) of bromeliad-impounded sediment was elevated relative to soil and gene surveys confirmed the presence of both chitinases and nitrogenases, suggesting that bromeliad tanks may provide important habitats for microbes involved in the biological cycling of carbon and nitrogen in tropical forests.

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