Biogeochemical activity and associated biodiversity at reduced deep-sea hotspot ecosystems

Abstract

Understanding biodiversity and its patterns across space, time and environmental gradients is central in order to assess the functioning of natural systems and their resilience to external perturbations. To date, the deep-sea floor and its associated ecosystems remain one of least explored environments on Earth, hence, little is known about their biodiversity, and especially that of microbes. Here we investigated the biogeochemical activity and associated bacterial biodiversity of two hotspot ecosystems in the deep-sea, the cold seeps and wood falls. Cold seeps and wood falls are peculiar ecosystems at the deep-sea floor, at which unique sources of energy such as methane and wood-derived cellulose fuel high biomasses of faunal communities with special diversity, typically not encountered at the deep-sea floor. In this study we specifically focused on the investigation of microbial communities since on one hand their diversity patterns are the least understood, and also because their capabilities to utilize methane and cellulose are crucial for the supply of energy to these ecosystems. Cold seeps and wood falls are isolated and fractured ecosystems with only small areal coverage, which poses a challenge for the dispersal of their associated communities and maintenance of their populations. The interconnectivity of these isolated ecosystems and the biodiversity patterns of microbes across different spatial scales are largely unknown. The combination of molecular fingerprinting and geochemical approaches used in this study helped to understand how microbial communities of seep and wood falls are connected over different spatial scales and identify the main environmental factors shaping their diversity. In Chapter I the local-scale patterns of bacterial community structure and their relation to the sediment heterogeneity was investigated at the REGAB cold seep pockmark. Strong variations in the sediment geochemistry and the core biogeochemical processes were detected between different reduced habitats, which were related to differences in the methane effluxes that ranged over two orders of magnitude. Variation in the structure of bacterial communities was linked to local sediment heterogeneity. Methane, the main energy source at cold seeps, was identified as the most important factor that shaped the seep bacterial community structure and distributions of chemosynthetic megafauna. The link between the relative abundance of symbiotic bacteria in the gills of a cold seep chemosynthetic mussel and their energy sources was investigated in Chapter II. Mussels inhabiting gassy sediments laden with methane had relatively higher abundance of methanotrophic symbionts that take up methane, in comparison to thiotrophic symbionts that rely on sulfide as their source of energy. In addition, the abundances of methanotrophs seemed to be linked to variations in methane concentrations in the bottom water, and were correlated with the content of methane-derived carbon in the mussel biomass. The results presented in Chapter III reveal how seep bacterial communities vary on local and regional scales, within and between cold seep sites. Variation in the seep bacterial community was not correlated to geographic distance, and instead communities displayed patchy structure reflecting on the variability in the sulfide content, as their main energy source. Highest bacterial turnover, with > 50% replacement with new bacterial types was evident between reduced habitats, separated by few meters to hundreds of meters. This result suggest that small reduced habitats, not more than few meters in diameter, represent biodiversity hotspots and contribute substantially to the overall diversity of the deep-sea floor. In the last chapter (IV) the temporal and spatial variations of communities associated to wood falls were investigated using experimental wood deployments. The results of this study suggest that biogeography plays an important role for the composition of both bacteria and fauna of wood-associated communities. Temporal succession of bacterial and faunal communities occurred within a period of 1 to 2 y. During the whole immersion period the bacterial communities associated to the wood fall remained distinct from the surrounding background sediments, indicating that wood falls represent an important source of diversity in the deep-sea floor.