BIODIVERSITY AND ECOLOGY OF DEEP-SEA CHEMOSYNTHETIC COMMUNITIES

2013-Current

Arguably the most extreme ecological feature of the deep sea is the scarcity of energy (Smith et al., 2008). Photosynthesis is usually not supported at waters deeper than 200-300 m. Deep-sea communities thus, largely depend on the sinking organic matter produced thousands of meters above in photosynthetic surface layers. Forty years ago, scientists observed for the very first time hydrothermal vents (at that time “hot springs”) at the Galapagos Spreading Center (Lonsdale 1977; Corliss et al. 1979). There, seawater percolates through seafloor cracks and fissures, reacts with the ocean crust and forms the anoxic hydrothermal fluids characterized by high temperatures (up to 400ºC), and elevated concentrations of heavy metals and chemically reduced compounds (H2, CH4, H2S) (Le Bris et al. 2019). Microorganisms obtain their energy through the oxidation of these compounds, an energetic process known as chemosynthesis, which forms the trophic base of faunal assemblages with high abundances and biomass strikingly contrasting with the surrounding deep-sea soft-bottom habitats (Corliss et al.; 1979; Sievert and Vetriani, 2015). The recognition of vents as hotspots of productivity completely challenged the idea of a total deep-sea dependence on photosynthetic primary productivity of surface waters (German et al., 2011). Some invertebrates present symbiotic relationships with chemosynthetic microorganisms dominating biomass and creating biogenic habitats home to many other species, as corals do with microscopic algae in tropical reefs.

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Soon after the discovery of vents in 1977, other cognate communities were found in distinct reducing environments such as those created in cold seeps (Paull et al., 1984). Furthermore, large organic remains, such as wood and whale carcasses, were found to sustain chemosynthetic productivity and faunal overlap with vents and seeps (Smith et al. 1989; Bienhold et al. 2013). Indeed, cetacean carcasses and sunken wood are the largest organic parcels exported from surface waters and create conditions that support chemosynthesis for years and even decades (Bienhold et al. 2013; Smith et al. 2015). Although “wood” and “whale falls” are thought to be common, they have been only relatively well studied during the last 30 yr and have been much less studied than vents and seeps, especially in basins outside the Northeast Pacific Ocean (Smith et al. 2015). Carcasses and wood greatly impact small areas of the seafloor (up to ~100 m2), attracting opportunistic and specialized fauna and creating unique island-like habitats considered to be hot spots of biodiversity and sources of evolutionary novelty (Bienhold et al. 2013; Smith et al. 2015). The organic matter in enriched sediments around falls and within the wood and lipid-rich skeletons is degraded by microorganisms, which generate fluxes of reduced compounds as by-products of their metabolism (Treude et al. 2009).

Chemosynthetic bacteria and chemosymbiotic invertebrates that exploit these fluxes also occur in vents and seeps (Smith et al. 1989). Smith et al. (1989) proposed the Stepping-stone Hypothesis that states that organic falls may act as stepping stones for the dispersal of some vent fauna to new and distant habitats. Organic falls are also  interesting habitats because they represent an eco-evolutionary link between the shallow and deep sea (whale carcasses) and the land and the ocean (woods) (Smith et al. 2015; Judge and Barry, 2016). Indeed, evidences suggest that some of the most iconic vent foundation species, such as chemosynthetic mussels, likely evolved from shallow waters to the deep sea using organic falls as stepping stones (Distel et al. 2000).