Giant sponge grounds of Central Arctic seamounts are associated with extinct seep life.

The Central Arctic Ocean is one of the most oligotrophic oceans on Earth because of its sea-ice cover and short productive season. Nonetheless, across the peaks of extinct volcanic seamounts of the Langseth Ridge (87°N, 61°E), we observe a surprisingly dense benthic biomass. Bacteriosponges are the most abundant fauna within this community, with a mass of 460 g C m-2 and an estimated carbon demand of around 110 g C m-2 yr-1, despite export fluxes from regional primary productivity only sufficient to provide <1% of this required carbon. Observed sponge distribution, bulk and compound-specific isotope data of fatty acids suggest that the sponge microbiome taps into refractory dissolved and particulate organic matter, including remnants of an extinct seep community. The metabolic profile of bacteriosponge fatty acids and expressed genes indicate that autotrophic symbionts contribute significantly to carbon assimilation. We suggest that this hotspot ecosystem is unique to the Central Arctic and associated with extinct seep biota, once fueled by degassing of the volcanic mounts.

Effects of a deep-sea mining experiment on seafloor microbial communities and functions after 26 years.

Future supplies of rare minerals for global industries with high-tech products may depend on deep-sea mining. However, environmental standards for seafloor integrity and recovery from environmental impacts are missing. We revisited the only midsize deep-sea disturbance and recolonization experiment carried out in 1989 in the Peru Basin nodule field to compare habitat integrity, remineralization rates, and carbon flow with undisturbed sites. Plough tracks were still visible, indicating sites where sediment was either removed or compacted. Locally, microbial activity was reduced up to fourfold in the affected areas. Microbial cell numbers were reduced by ~50% in fresh "tracks" and by <30% in the old tracks. Growth estimates suggest that microbially mediated biogeochemical functions need over 50 years to return to undisturbed levels. This study contributes to developing environmental standards for deep-sea mining while addressing limits to maintaining and recovering ecological integrity during large-scale nodule mining.

In situ development of a methanotrophic microbiome in deep-sea sediments.

Emission of the greenhouse gas methane from the seabed is globally controlled by marine aerobic and anaerobic methanotrophs gaining energy via methane oxidation. However, the processes involved in the assembly and dynamics of methanotrophic populations in complex natural microbial communities remain unclear. Here we investigated the development of a methanotrophic microbiome following subsurface mud eruptions at Håkon Mosby mud volcano (1250 m water depth). Freshly erupted muds hosted deep-subsurface communities that were dominated by Bathyarchaeota, Atribacteria and Chloroflexi. Methanotrophy was initially limited to a thin surface layer of Methylococcales populations consuming methane aerobically. With increasing distance to the eruptive center, anaerobic methanotrophic archaea, sulfate-reducing Desulfobacterales and thiotrophic Beggiatoaceae developed, and their respective metabolic capabilities dominated the biogeochemical functions of the community. Microbial richness, evenness, and cell numbers of the entire microbial community increased up to tenfold within a few years downstream of the mud flow from the eruptive center. The increasing diversity was accompanied by an up to fourfold increase in sequence abundance of relevant metabolic genes of the anaerobic methanotrophic and thiotrophic guilds. The communities fundamentally changed in their structure and functions as reflected in the metagenome turnover with distance from the eruptive center, and this was reflected in the biogeochemical zonation across the mud volcano caldera. The observed functional succession provides a framework for the response time and recovery of complex methanotrophic communities after disturbances of the deep-sea bed.

Bacterial taxa-area and distance-decay relationships in marine environments.

The taxa-area relationship (TAR) and the distance-decay relationship (DDR) both describe spatial turnover of taxa and are central patterns of biodiversity. Here, we compared TAR and DDR of bacterial communities across different marine realms and ecosystems at the global scale. To obtain reliable global estimates for both relationships, we quantified the poorly assessed effects of sequencing depth, rare taxa removal and number of sampling sites. Slope coefficients of bacterial TARs were within the range of those of plants and animals, whereas slope coefficients of bacterial DDR were much lower. Slope coefficients were mostly affected by removing rare taxa and by the number of sampling sites considered in the calculations. TAR and DDR slope coefficients were overestimated at sequencing depth <4000 sequences per sample. Noticeably, bacterial TAR and DDR patterns did not correlate with each other both within and across ecosystem types, suggesting that (i) TAR cannot be directly derived from DDR and (ii) TAR and DDR may be influenced by different ecological factors. Nevertheless, we found marine bacterial TAR and DDR to be steeper in ecosystems associated with high environmental heterogeneity or spatial isolation, namely marine sediments and coastal environments compared with pelagic ecosystems. Hence, our study provides information on macroecological patterns of marine bacteria, as well as methodological and conceptual insights, at a time when biodiversity surveys increasingly make use of high-throughput sequencing technologies.

Relative abundances of methane- and sulphur-oxidising symbionts in the gills of a cold seep mussel and link to their potential energy sources.

Bathymodiolus mussels are key species in many deep-sea chemosynthetic ecosystems. They often harbour two types of endosymbiotic bacteria in their gills, sulphur- and methane oxidisers. These bacteria take up sulphide and methane from the environment and provide energy to their hosts, supporting some of the most prolific ecosystems in the sea. In this study, we tested whether symbiont relative abundances in Bathymodiolus gills reflect variations in the highly spatially dynamic chemical environment of cold seep mussels. Samples of Bathymodiolus aff. boomerang were obtained from two cold seeps of the deep Gulf of Guinea, REGAB (5°47.86S, 9°42.69E, 3170 m depth) and DIAPIR (6°41.58S, 10°20.94E, 2700 m depth). Relative abundances of both symbiont types were measured by means of 3D fluorescence in situ hybridisation and image analysis and compared considering the local sulphide and methane concentrations and fluxes assessed via benthic chamber incubations. Specimens inhabiting areas with highest methane content displayed higher relative abundances of methane oxidisers. The bacterial abundances correlated also with carbon stable isotope signatures in the mussel tissue, suggesting a higher contribution of methane-derived carbon to the biomass of mussels harbouring higher densities of methane-oxidising symbionts. A dynamic adaptation of abundances of methanotrophs and thiotrophs in the gill could be a key factor optimising the energy yield for the symbiotic system and could explain the success of dual symbiotic mussels at many cold seeps and hydrothermal vents of the Atlantic and Gulf of Mexico.

Niche differentiation among mat-forming, sulfide-oxidizing bacteria at cold seeps of the Nile Deep Sea Fan (Eastern Mediterranean Sea).

Sulfidic muds of cold seeps on the Nile Deep Sea Fan (NDSF) are populated by different types of mat-forming sulfide-oxidizing bacteria. The predominant sulfide oxidizers of three different mats were identified by microscopic and phylogenetic analyses as (i) Arcobacter species producing cotton-ball-like sulfur precipitates, (ii) large filamentous sulfur bacteria including Beggiatoa species, and (iii) single, spherical Thiomargarita species. High resolution in situ microprofiles revealed different geochemical settings selecting for the different mat types. Arcobacter mats occurred where oxygen and sulfide overlapped above the seafloor in the bottom water interface. Filamentous sulfide oxidizers were associated with steep gradients of oxygen and sulfide in the sediment. A dense population of Thiomargarita was favored by temporarily changing supplies of oxygen and sulfide in the bottom water. These results indicate that the decisive factors in selecting for different mat-forming bacteria within one deep-sea province are spatial or temporal variations in energy supply. Furthermore, the occurrence of Arcobacter spp.-related 16S rRNA genes in the sediments below all three types of mats, as well as on top of brine lakes of the NDSF, indicates that this group of sulfide oxidizers can switch between different life modes depending on the geobiochemical habitat setting.

Impact of space, time and complex environments on microbial communities.

The unparalleled accumulation of biological and contextual data is currently revolutionizing the way environmental microbiologists address ecological questions. Here, we briefly review the likely causes that may explain this remarkable scientific revolution and present a synthesized view about how to describe microbial communities in their complex environmental context.

In situ experimental evidence of the fate of a phytodetritus pulse at the abyssal sea floor.

More than 50% of the Earth' s surface is sea floor below 3,000 m of water. Most of this major reservoir in the global carbon cycle and final repository for anthropogenic wastes is characterized by severe food limitation. Phytodetritus is the major food source for abyssal benthic communities, and a large fraction of the annual food load can arrive in pulses within a few days. Owing to logistical constraints, the available data concerning the fate of such a pulse are scattered and often contradictory, hampering global carbon modelling and anthropogenic impact assessments. We quantified (over a period of 2.5 to 23 days) the response of an abyssal benthic community to a phytodetritus pulse, on the basis of 11 in situ experiments. Here we report that, in contrast to previous hypotheses, the sediment community oxygen consumption doubled immediately, and that macrofauna were very important for initial carbon degradation. The retarded response of bacteria and Foraminifera, the restriction of microbial carbon degradation to the sediment surface, and the low total carbon turnover distinguish abyssal from continental-slope 'deep-sea' sediments.

A marine microbial consortium apparently mediating anaerobic oxidation of methane.

A large fraction of globally produced methane is converted to CO2 by anaerobic oxidation in marine sediments. Strong geochemical evidence for net methane consumption in anoxic sediments is based on methane profiles, radiotracer experiments and stable carbon isotope data. But the elusive microorganisms mediating this reaction have not yet been isolated, and the pathway of anaerobic oxidation of methane is insufficiently understood. Recent data suggest that certain archaea reverse the process of methanogenesis by interaction with sulphate-reducing bacteria. Here we provide microscopic evidence for a structured consortium of archaea and sulphate-reducing bacteria, which we identified by fluorescence in situ hybridization using specific 16S rRNA-targeted oligonucleotide probes. In this example of a structured archaeal-bacterial symbiosis, the archaea grow in dense aggregates of about 100 cells and are surrounded by sulphate-reducing bacteria. These aggregates were abundant in gas-hydrate-rich sediments with extremely high rates of methane-based sulphate reduction, and apparently mediate anaerobic oxidation of methane.