Symbiotic adaptation of prokaryotic microorganisms in extreme deep-sea environments

Extreme deep-sea environments are widespread and intensively studied in the last decades. They are of special interest since living organisms in those habitats happen to live at the expenses of the fluids emitted from the subseafloor via chemosynthesis. Unlike most common ecosystems, which rely on photosynthesis, primary producers obtain their carbon and energy sources through chemical reactions, i. e. sulfide oxidation, sulfate reduction, methane oxidation. Furthermore, the conditions given in hydrothermal vents are similar to those given in primitive Earth and metabolisms found in these ecosystems may provide information about the first metabolisms on Earth (origin of life is estimated to have occurred ca. 3.6 – 4 Ga years ago). For instance, methanogenesis (abundant in hydrothermal vents and also present in cold seeps) is considered a good candidate for being the metabolism driven by the last unique common ancestor (LUCA), since the process of serpentinization observed in alkaline hydrothermal fields is capable of producing hydrogen (H2) abiotically. Furthermore, anaerobic oxidation of methane (AOM) may have also appeared in the early Archaean, although earliest evidences date from 2.7 Ga years ago and it seems this metabolism was not stable until shortly before the Great Oxidation Event (ca. 2.4 Ga ago). Nowadays, AOM is the major sink of methane in deep-sea oceans, driven by a symbiotic relationship between ANME archaea and SRB bacteria. Extreme deep-sea environments are also characterized by the common presence of certain clades of marine invertebrates (mostly tubeworms and bivalves). DNA analysis performed on organisms living in modern hydrothermal vents and cold seeps point out that their ancestors belong to shallower waters, indicating they have colonized the deep-sea more recently. Therefore, for these organisms to live in these reduced environments is harsh and they have adapted to low oxygen, high pressure and extreme temperatures. Interestingly, intensive studies performed on these animals have revealed they harbor in their organs chemosynthetic endosymbionts. These prokaryotes provide with organics the invertebrates, while they enjoy the easy access to the metabolites needed for chemosynthesis. In this study, we analyze the symbiotic adaptation of prokaryotes in extreme deep-sea environments. To do so, we have sampled mud volcanoes in the Gulf of Cádiz for further understanding of this relationship between organisms. In the first chapter, we have focused on the existing relationship between cold-water corals and seepage of fluids in the Pompeia Province, since they are found related to active seepage and there is no evidence of a chemosynthetic life-style of the corals. Results indicate that the corals use AOM-derived carbonates as the hard substrata they need to settle and flourish. Furthermore, they are capable of living upon seeping fluids by means of chemosynthetic microorganisms, i. e. AOM-related microorganisms, siboglinids, and sulfide-oxidizing bacterial mats, which feed on the emitted fluids and protect the corals — the so-called the buffer effect. The second chapter is focused on the finding of small Siboglinidae worms in four different mud volcanoes in the Gulf of Cádiz (El Cid MV, Bonjardim MV, Al Gacel MV and Anastasya MV). Although not all of them were alive, tubes recovered from those volcanoes currently active (Al Gacel MV and Anastasya MV) harbored a microbial biofilm related to them. This finding suggests that the worms’ microbiota is more extended as previously thought. Furthermore, DNA analyses revealed changes in the worms’ microbiota depending on the mud volcano, i. e. depending on the seepage activity. Due to the common observations of symbiosis in the Gulf of Cádiz and other extreme deep-sea environments, we aim to elucidate the importance of symbiosis not only in these ecosystems but in the history of evolution. To do so we have collected data from our study and other reported studies to have a better and global understanding of the role of symbiosis in evolution. We have concluded that symbiosis is indeed a major motor in evolution and therefore evolutionary and theoretical biology needs to re-think the basis of the actual theory of evolution