Temperatures around hydrothermal vents are highly variable, ranging from near freezing up to 3008C. Nevertheless, animals thrive around vents, some of which live near the known limits of animal thermotolerance. Paralvinella sulfincola, an extremely thermotolerant vent polychaete, and Paralvinella palmiformis, a cooleradapted congener, are found along the Juan de Fuca Ridge in the northwestern Pacific. We conducted shipboard high-pressure thermotolerance experiments on both species to characterize the physiological adaptations underlying P. sulfincola's pronounced thermotolerance. Quantitative proteomics, expressed sequence tag (EST) libraries and glutathione assays revealed that P. sulfincola (i) exhibited an upregulation in the synthesis and recycling of glutathione with increasing temperature, (ii) downregulated nicotinamide adenine dinucleotide (NADH) and succinate dehydrogenases (key enzymes in oxidative phosphorylation) with increasing temperature, and (iii) maintained elevated levels of heat shock proteins (HSPs) across all treatments. In contrast, P. palmiformis exhibited more typical responses to increasing temperatures (e.g. increasing HSPs at higher temperatures). These data reveal differences in how a mesotolerant and extremely thermotolerant eukaryote respond to thermal stress, and suggest that P. sulfincola's capacity to mitigate oxidative stress via increased synthesis of antioxidants and decreased flux through the mitochondrial electron transport chain enable pronounced thermotolerance. Ultimately, oxidative stress may be the key factor in limiting all metazoan thermotolerance.
Marine microbial communities are highly interconnected assemblages of organisms shaped by ecological drift, natural selection, and dispersal. The relative strength of these forces determines how ecosystems respond to environmental gradients, how much diversity is resident in a community or population at any given time, and how populations reorganize and evolve in response to environmental perturbations. In this study, we introduce a globally resolved population–genetic ocean model in order to examine the interplay of dispersal, selection, and adaptive evolution and their effects on community assembly and global biogeography. We find that environmental selection places strong constraints on global dispersal, even in the face of extremely high assumed rates of adaptation. Changing the relative strengths of dispersal, selection, and adaptation has pronounced effects on community assembly in the model and suggests that barriers to dispersal play a key role in the structuring of marine communities, enhancing global biodiversity and the importance of local historical contingencies.
Many foundation species in chemosynthesis-based ecosystems rely on environmentally acquired symbiotic bacteria for their survival. Hence, understanding the biogeographic distributions of these symbionts at regional scales is key to understanding patterns of connectivity and predicting resilience of their host populations (and thus whole communities). However, such assessments are challenging because they necessitate measuring bacterial genetic diversity at fine resolutions. For this purpose, the recently discovered clustered regularly interspaced short palindromic repeats (CRISPR) constitutes a promising new genetic marker. These DNA sequences harboured by about half of bacteria hold their viral immune memory, and as such, might allow discrimination of different lineages or strains of otherwise indistinguishable bacteria. In this study, we assessed the potential of CRISPR as a hypervariable phylogenetic marker in the context of a population genetic study of an uncultured bacterial species. We used high-throughput CRISPR-based typing along with multi-locus sequence analysis (MLSA) to characterize the regional population structure of the obligate but environmentally acquired symbiont species Candidatus Endoriftia persephone on the Juan de Fuca Ridge. Mixed symbiont populations of Ca. Endoriftia persephone were sampled across individual Ridgeia piscesae hosts from contrasting habitats in order to determine if environmental conditions rather than barriers to connectivity are more important drivers of symbiont diversity. We showed that CRISPR revealed a much higher symbiont genetic diversity than the other housekeeping genes. Several lines of evidence imply this diversity is indicative of environmental strains. Finally, we found with both CRISPR and gene markers that local symbiont populations are strongly differentiated across sites known to be isolated by deep-sea circulation patterns. This research showed the high power of CRISPR to resolve the genetic structure of uncultured bacterial populations and represents a step towards making keystone microbial species an integral part of conservation policies for upcoming mining operations on the seafloor.
Abyssal microbes drive biogeochemical cycles, regulate fluxes of energy and contribute to organic carbon production and remineralization. Therefore, characterizing the spatial variability of benthic microbes is important for understanding their roles in benthic environments and for conducting baseline assessments of areas of the seabed that might be targeted by commercial mining activities. Yet, detailed assessments of the spatial distributions of benthic microbial communities in these regions are still incomplete, and these efforts have not yet considered the influence of seafloor topography and heterogeneity on microbial distributions across a range of scales. In this study, we investigated the composition and spatial variability of benthic microbial assemblages found in sediments and polymetallic nodules collected from the Clarion Clipperton Zone (CCZ) in the equatorial Pacific (4000–4300 m water depth). We used 16S rRNA gene sequences to characterize these communities. The upper 20 cm of abyssal sediments harbored diverse and distinctive microbial communities in both sediments and their associated polymetallic nodules, with high similarity across topographical areas of the seabed. Assemblage composition differed vertically through the sediment, by habitat and across small to mesoscales. Potential carbon-fixing microbes formed more than 25% relative abundance of sediment assemblages, which were dominated by ammonia-oxidizing Archaea Nitrosopumilus. Non-photosynthetic Cyanobacteria were more frequent in the deeper sediment layers and nodules. Sediment communities had a higher abundance of taxa involved in nitrogen cycling, such as Nitrosopumilus, Nitrospina, Nitrospira, AqS1 (Nitrosococcaceae), and methanogens wb1-A12 (NC10 phylum). In contrast, nodules were more enriched in Alphaproteobacteria, Gammaproteobacteria, Planctomycetes, Acidobacteria, Bacteroidetes, Nanoarchaeaeota, and Calditrichaeota. Microbes related to potential metal-cycling (Magnetospiraceae and Kiloniellaceae), organic carbon remineralization (Woeseia), and sulfur-oxidizing Thiohalorhabdaceae were also more enriched in nodules. Our results indicate that benthic microbial community composition is driven by sediment profile depth and seafloor heterogeneity at small and mesoscales. The most abundant microbial taxa within the sediments were nitrifying and putative carbon-fixing microbes, and may have key ecological roles in mediating biogeochemical cycles in this habitat.
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