Temporal and Spatial Variations of Bacterial and Faunal Communities Associated with Deep-Sea Wood Falls.
ABSTRACT: Sinking of large organic food falls i.e. kelp, wood and whale carcasses to the oligotrophic deep-sea floor promotes the establishment of locally highly productive and diverse ecosystems, often with specifically adapted benthic communities. However, the fragmented spatial distribution and small area poses challenges for the dispersal of their microbial and faunal communities. Our study focused on the temporal dynamics and spatial distributions of sunken wood bacterial communities, which were deployed in the vicinity of different cold seeps in the Eastern Mediterranean and the Norwegian deep-seas. By combining fingerprinting of bacterial communities by ARISA and 454 sequencing with in situ and ex situ biogeochemical measurements, we show that sunken wood logs have a locally confined long-term impact (> 3y) on the sediment geochemistry and community structure. We confirm previous hypotheses of different successional stages in wood degradation including a sulphophilic one, attracting chemosynthetic fauna from nearby seep systems. Wood experiments deployed at similar water depths (1100-1700 m), but in hydrographically different oceanic regions harbored different wood-boring bivalves, opportunistic faunal communities, and chemosynthetic species. Similarly, bacterial communities on sunken wood logs were more similar within one geographic region than between different seas. Diverse sulphate-reducing bacteria of the Deltaproteobacteria, the sulphide-oxidizing bacteria Sulfurovum as well as members of the Acidimicrobiia and Bacteroidia dominated the wood falls in the Eastern Mediterranean, while Alphaproteobacteria and Flavobacteriia colonized the Norwegian Sea wood logs. Fauna and bacterial wood-associated communities changed between 1 to 3 years of immersion, with sulphate-reducers and sulphide-oxidizers increasing in proportion, and putative cellulose degraders decreasing with time. Only 6% of all bacterial genera, comprising the core community, were found at any time on the Eastern Mediterranean sunken wooden logs. This study suggests that biogeography and succession play an important role for the composition of bacteria and fauna of wood-associated communities, and that wood can act as stepping-stones for seep biota.
Project description:Large organic food falls to the deep sea--such as whale carcasses and wood logs--are known to serve as stepping stones for the dispersal of highly adapted chemosynthetic organisms inhabiting hot vents and cold seeps. Here we investigated the biogeochemical and microbiological processes leading to the development of sulfidic niches by deploying wood colonization experiments at a depth of 1690 m in the Eastern Mediterranean for one year. Wood-boring bivalves of the genus Xylophaga played a key role in the degradation of the wood logs, facilitating the development of anoxic zones and anaerobic microbial processes such as sulfate reduction. Fauna and bacteria associated with the wood included types reported from other deep-sea habitats including chemosynthetic ecosystems, confirming the potential role of large organic food falls as biodiversity hot spots and stepping stones for vent and seep communities. Specific bacterial communities developed on and around the wood falls within one year and were distinct from freshly submerged wood and background sediments. These included sulfate-reducing and cellulolytic bacterial taxa, which are likely to play an important role in the utilization of wood by chemosynthetic life and other deep-sea animals.
Project description:The cornerstones of sunken wood ecosystems are microorganisms involved in cellulose degradation. These can either be free-living microorganisms in the wood matrix or symbiotic bacteria associated with wood-boring bivalves such as emblematic species of Xylophaga, the most common deep-sea woodborer. Here we use experimentally submerged pine wood, placed in and outside the Mediterranean submarine Blanes Canyon, to compare the microbial communities on the wood, in fecal pellets of Xylophaga spp. and associated with the gills of these animals. Analyses based on tag pyrosequencing of the 16S rRNA bacterial gene showed that sunken wood contained three distinct microbial communities. Wood and pellet communities were different from each other suggesting that Xylophaga spp. create new microbial niches by excreting fecal pellets into their burrows. In turn, gills of Xylophaga spp. contain potential bacterial symbionts, as illustrated by the presence of sequences closely related to symbiotic bacteria found in other wood eating marine invertebrates. Finally, we found that sunken wood communities inside the canyon were different and more diverse than the ones outside the canyon. This finding extends to the microbial world the view that submarine canyons are sites of diverse marine life.
Project description:The methane-emitting cold seeps of Hikurangi margin (New Zealand) are among the few deep-sea chemosynthetic ecosystems of the Southern Hemisphere known to date. Here we compared the biogeochemistry and microbial communities of a variety of Hikurangi cold seep ecosystems. These included highly reduced seep habitats dominated by bacterial mats, partially oxidized habitats populated by heterotrophic ampharetid polychaetes and deeply oxidized habitats dominated by chemosynthetic frenulate tubeworms. The ampharetid habitats were characterized by a thick oxic sediment layer that hosted a diverse and biomass-rich community of aerobic methanotrophic Gammaproteobacteria. These bacteria consumed up to 25% of the emanating methane and clustered within three deep-branching groups named Marine Methylotrophic Group (MMG) 1-3. MMG1 and MMG2 methylotrophs belong to the order Methylococcales, whereas MMG3 methylotrophs are related to the Methylophaga. Organisms of the groups MMG1 and MMG3 are close relatives of chemosynthetic endosymbionts of marine invertebrates. The anoxic sediment layers of all investigated seeps were dominated by anaerobic methanotrophic archaea (ANME) of the ANME-2 clade and sulfate-reducing Deltaproteobacteria. Microbial community analysis using Automated Ribosomal Intergenic Spacer Analysis (ARISA) showed that the different seep habitats hosted distinct microbial communities, which were strongly influenced by the seep-associated fauna and the geographic location. Despite outstanding features of Hikurangi seep communities, the organisms responsible for key ecosystem functions were similar to those found at seeps worldwide. This suggests that similar types of biogeochemical settings select for similar community composition regardless of geographic distance. Because ampharetid polychaetes are widespread at cold seeps the role of aerobic methanotrophy may have been underestimated in seafloor methane budgets.
Project description:Cold seeps are highly productive, fragmented marine ecosystems that form at the seafloor around hydrocarbon emission pathways. The products of microbial utilization of methane and other hydrocarbons fuel rich chemosynthetic communities at these sites, with much higher respiration rates compared with the surrounding deep-sea floor. Yet little is known as to the richness, composition and spatial scaling of bacterial communities of cold seeps compared with non-seep communities. Here we assessed the bacterial diversity across nine different cold seeps in the Eastern Mediterranean deep-sea and surrounding seafloor areas. Community similarity analyses were carried out based on automated ribosomal intergenic spacer analysis (ARISA) fingerprinting and high-throughput 454 tag sequencing and were combined with in situ and ex situ geochemical analyses across spatial scales of a few tens of meters to hundreds of kilometers. Seep communities were dominated by Deltaproteobacteria, Epsilonproteobacteria and Gammaproteobacteria and shared, on average, 36% of bacterial types (ARISA OTUs (operational taxonomic units)) with communities from nearby non-seep deep-sea sediments. Bacterial communities of seeps were significantly different from those of non-seep sediments. Within cold seep regions on spatial scales of only tens to hundreds of meters, the bacterial communities differed considerably, sharing <50% of types at the ARISA OTU level. Their variations reflected differences in porewater sulfide concentrations from anaerobic degradation of hydrocarbons. This study shows that cold seep ecosystems contribute substantially to the microbial diversity of the deep-sea.
Project description:One of the most striking features of modern chemosynthesis-based ecosystems surrounding methane seeps is the presence of abundant chemosymbiotic bivalves. However, such accumulations have rarely been reported from Palaeozoic to mid-Mesozoic seeps, and it is widely thought that general trends in the evolution of chemosynthetic communities paralleled those typifying most marine environments, with the bivalve prevalence starting in the Mesozoic and with Palaeozoic seeps being dominated by brachiopods. Here, we report a discovery of bivalve clusters in the oldest-known methane seep that hosted metazoan fauna, dated to the late Silurian. We identify the bivalves, externally very similar to modern chemosymbiotic forms, as members of the extinct family Modiomorphidae, known previously from a younger, Devonian seep. The bivalves inhabited the seep at a stage of increased fluid flow, when they co-occurred with atrypid brachiopods, and display a set of morphological characteristics suggesting a seep-obligate lifestyle. We conclude that bivalves colonised chemosynthesis-based ecosystems at least as early as brachiopods and apparently first developed specialized lineages able to thrive in seep-related habitats for a prolonged period of time. Rather than being simple ecological successors of brachiopods, rich bivalve communities represent an ancient and recurring theme in the evolution of chemosynthetic assemblages.
Project description:Mussels of the genus Bathymodiolus are among the most widespread colonizers of hydrothermal vent and cold seep environments, sustained by endosymbiosis with chemosynthetic bacteria. Presumed species of Bathymodiolus are abundant at newly discovered cold seeps on the Mid-Atlantic continental slope, however morphological taxonomy is challenging, and their phylogenetic affinities remain unestablished. Here we used mitochondrial sequence to classify species found at three seep sites (Baltimore Canyon seep (BCS; ~400m); Norfolk Canyon seep (NCS; ~1520m); and Chincoteague Island seep (CTS; ~1000m)). Mitochondrial COI (N = 162) and ND4 (N = 39) data suggest that Bathymodiolus childressi predominates at these sites, although single B. mauritanicus and B. heckerae individuals were detected. As previous work had suggested that methanotrophic and thiotrophic interactions can both occur at a site, and within an individual mussel, we investigated the symbiont communities in gill tissues of a subset of mussels from BCS and NCS. We constructed metabarcode libraries with four different primer sets spanning the 16S gene. A methanotrophic phylotype dominated all gill microbial samples from BCS, but sulfur-oxidizing Campylobacterota were represented by a notable minority of sequences from NCS. The methanotroph phylotype shared a clade with globally distributed Bathymodiolus spp. symbionts from methane seeps and hydrothermal vents. Two distinct Campylobacterota phylotypes were prevalent in NCS samples, one of which shares a clade with Campylobacterota associated with B. childressi from the Gulf of Mexico and the other with Campylobacterota associated with other deep-sea fauna. Variation in chemosynthetic symbiont communities among sites and individuals has important ecological and geochemical implications and suggests shifting reliance on methanotrophy. Continued characterization of symbionts from cold seeps will provide a greater understanding of the ecology of these unique environments as well and their geochemical footprint in elemental cycling and energy flux.
Project description:Wood falls on the ocean floor form chemosynthetic ecosystems that remain poorly studied compared with features such as hydrothermal vents or whale falls. In particular, the microbes forming the base of this unique ecosystem are not well characterized and the ecology of communities is not known. Here we use wood as a model to study microorganisms that establish and maintain a chemosynthetic ecosystem. We conducted both aquaria and in situ deep-sea experiments to test how different environmental constraints structure the assembly of bacterial, archaeal and fungal communities. We also measured changes in wood lipid concentrations and monitored sulfide production as a way to detect potential microbial activity. We show that wood falls are dynamic ecosystems with high spatial and temporal community turnover, and that the patterns of microbial colonization change depending on the scale of observation. The most illustrative example was the difference observed between pine and oak wood community dynamics. In pine, communities changed spatially, with strong differences in community composition between wood microhabitats, whereas in oak, communities changed more significantly with time of incubation. Changes in community assembly were reflected by changes in phylogenetic diversity that could be interpreted as shifts between assemblies ruled by species sorting to assemblies structured by competitive exclusion. These ecological interactions followed the dynamics of the potential microbial metabolisms accompanying wood degradation in the sea. Our work showed that wood is a good model for creating and manipulating chemosynthetic ecosystems in the laboratory, and attracting not only typical chemosynthetic microbes but also emblematic macrofaunal species.
Project description:In the Guaymas Basin, the presence of cold seeps and hydrothermal vents in close proximity, similar sedimentary settings and comparable depths offers a unique opportunity to assess and compare the functioning of these deep-sea chemosynthetic ecosystems. The food webs of five seep and four vent assemblages were studied using stable carbon and nitrogen isotope analyses. Although the two ecosystems shared similar potential basal sources, their food webs differed: seeps relied predominantly on methanotrophy and thiotrophy via the Calvin-Benson-Bassham (CBB) cycle and vents on petroleum-derived organic matter and thiotrophy via the CBB and reductive tricarboxylic acid (rTCA) cycles. In contrast to symbiotic species, the heterotrophic fauna exhibited high trophic flexibility among assemblages, suggesting weak trophic links to the metabolic diversity of chemosynthetic primary producers. At both ecosystems, food webs did not appear to be organised through predator-prey links but rather through weak trophic relationships among co-occurring species. Examples of trophic or spatial niche differentiation highlighted the importance of species-sorting processes within chemosynthetic ecosystems. Variability in food web structure, addressed through Bayesian metrics, revealed consistent trends across ecosystems. Food-web complexity significantly decreased with increasing methane concentrations, a common proxy for the intensity of seep and vent fluid fluxes. Although high fluid-fluxes have the potential to enhance primary productivity, they generate environmental constraints that may limit microbial diversity, colonisation of consumers and the structuring role of competitive interactions, leading to an overall reduction of food-web complexity and an increase in trophic redundancy. Heterogeneity provided by foundation species was identified as an additional structuring factor. According to their biological activities, foundation species may have the potential to partly release the competitive pressure within communities of low fluid-flux habitats. Finally, ecosystem functioning in vents and seeps was highly similar despite environmental differences (e.g. physico-chemistry, dominant basal sources) suggesting that ecological niches are not specifically linked to the nature of fluids. This comparison of seep and vent functioning in the Guaymas basin thus provides further supports to the hypothesis of continuity among deep-sea chemosynthetic ecosystems.
Project description:Like hydrothermal vents along oceanic ridges, cold seeps are patchy and isolated ecosystems along continental margins, extending from bathyal to abyssal depths. The Atlantic Equatorial Belt (AEB), from the Gulf of Mexico to the Gulf of Guinea, was one focus of the Census of Marine Life ChEss (Chemosynthetic Ecosystems) program to study biogeography of seep and vent fauna. We present a review and analysis of collections from five seep regions along the AEB: the Gulf of Mexico where extensive faunal sampling has been conducted from 400 to 3300 m, the Barbados accretionary prism, the Blake ridge diapir, and in the Eastern Atlantic from the Congo and Gabon margins and the recently explored Nigeria margin. Of the 72 taxa identified at the species level, a total of 9 species or species complexes are identified as amphi-Atlantic. Similarity analyses based on both Bray Curtis and Hellinger distances among 9 faunal collections, and principal component analysis based on presence/absence of megafauna species at these sites, suggest that within the AEB seep megafauna community structure is influenced primarily by depth rather than by geographic distance. Depth segregation is observed between 1000 and 2000 m, with the middle slope sites either grouped with those deeper than 2000 m or with the shallower sites. The highest level of community similarity was found between the seeps of the Florida escarpment and Congo margin. In the western Atlantic, the highest degree of similarity is observed between the shallowest sites of the Barbados prism and of the Louisiana slope. The high number of amphi-atlantic cold-seep species that do not cluster according to biogeographic regions, and the importance of depth in structuring AEB cold-seep communities are the major conclusions of this study. The hydrothermal vent sites along the Mid Atlantic Ridge (MAR) did not appear as "stepping stones" for dispersal of the AEB seep fauna, however, the south MAR and off axis regions should be further explored to more fully test this hypothesis.
Project description:Reducing conditions with elevated sulfide and methane concentrations in ecosystems such as hydrothermal vents, cold seeps or organic falls, are suitable for chemosynthetic primary production. Understanding processes driving bacterial diversity, colonization and dispersal is of prime importance for deep-sea microbial ecology. This study provides a detailed characterization of bacterial assemblages colonizing plant-derived substrates using a standardized approach over a geographic area spanning the North-East Atlantic and Mediterranean. Wood and alfalfa substrates in colonization devices were deployed for different periods at 8 deep-sea chemosynthesis-based sites in four distinct geographic areas. Pyrosequencing of a fragment of the 16S rRNA-encoding gene was used to describe bacterial communities. Colonization occurred within the first 14 days. The diversity was higher in samples deployed for more than 289 days. After 289 days, no relation was observed between community richness and deployment duration, suggesting that diversity may have reached saturation sometime in between. Communities in long-term deployments were different, and their composition was mainly influenced by the geographical location where devices were deployed. Numerous sequences related to horizontally-transmitted chemosynthetic symbionts of metazoans were identified. Their potential status as free-living forms of these symbionts was evaluated based on sequence similarity with demonstrated symbionts. Results suggest that some free-living forms of metazoan symbionts or their close relatives, such as Epsilonproteobacteria associated with the shrimp Rimicaris exoculata, are efficient colonizers of plant substrates at vents and seeps.