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Microbial Ecology of Deep-Sea Hypersaline Anoxic Basins

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Microbial Ecology of Deep-Sea Hypersaline Anoxic Basins Microbial ecology of deep-sea hypersaline anoxic basins Item Type Article Authors Merlino, Giuseppe; Barozzi, Alan; Michoud, Gregoire; Ngugi, David; Daffonchio, Daniele Citation Merlino G, Barozzi A, Michoud G, Ngugi DK, Daffonchio D (2018) Microbial ecology of deep-sea hypersaline anoxic basins. FEMS Microbiology Ecology. Available: http://dx.doi.org/10.1093/ femsec/fiy085. Eprint version Post-print DOI 10.1093/femsec/fiy085 Publisher Oxford University Press (OUP) Journal FEMS Microbiology Ecology Rights This is a pre-copyedited, author-produced PDF of an article accepted for publication in FEMS Microbiology Ecology following peer review. The version of record is available online at: https:// academic.oup.com/femsec/advance-article/doi/10.1093/femsec/ fiy085/4995905. Download date 25/09/2021 08:30:46 Link to Item http://hdl.handle.net/10754/627936 Microbial ecology of deep-sea hypersaline anoxic basins Giuseppe Merlino, Alan Barozzi, Grégoire Michoud, David Kamanda Ngugi, and Daniele Daffonchio*,† King Abdullah University of Science and Technology (KAUST), Red Sea Research Center (RSRC), Thuwal 23955-6900, Saudi Arabia *Corresponding authors: King Abdullah University of Science and Technology (KAUST), Biological and Environmental Sciences and Engineering Division (BESE), Thuwal, 23955- 6900, Saudi Arabia. Phone: +966 (12) 8082884; E-mail: [email protected]. One sentence summary: The last twenty years investigations on the deep hypersaline anoxic basins at the bottom of the oceans have revealed a complex microbial ecology with very diverse and unique metabolisms. † Daniele Daffonchio, http://orcid.org/0000-0003-0947-925X Abstract Deep hypersaline anoxic basins (DHABs) are unique water bodies occurring within fractures at the bottom of the sea, where the dissolution of anciently buried evaporites created dense anoxic brines that are separated by a chemocline/pycnocline from the overlying oxygenated deep-seawater column. DHABs have been described in the Gulf of Mexico, the Mediterranean Sea, the Black Sea and the Red Sea. They are characterized by prolonged Downloaded from https://academic.oup.com/femsec/advance-article-abstract/doi/10.1093/femsec/fiy085/4995905 by King Abdullah University of Science and Technology user on 20 May 2018 historical separation of the brines from the upper water column due to lack of mixing and by extreme conditions of salinity, anoxia, and relatively high hydrostatic pressure and temperatures. Due to these combined selection factors, unique microbial assemblages thrive in these polyextreme ecosystems. The topological localization of the different taxa in the brine-seawater transition zone coupled with the metabolic interactions and niche adaptations determine the metabolic functioning and biogeochemistry of DHABs. In particular, inherent metabolic strategies accompanied by genetic adaptations have provided insights on how prokaryotic communities can adapt to salt-saturated condition. Here, we review the current knowledge on the diversity, genomics, metabolisms and ecology of prokaryotes in DHABs. Keywords: DHABs; microbial diversity; microbial ecology; element cycles; Red Sea. Introduction Among the most extreme places, where microbial life has been reported, are the so-called deep hypersaline anoxic basins (DHABs, Mapelli et al. 2017a). Since the observation of the hot-brine-filled Atlantis II Deep at the bottom of the Red Sea (Charnock 1964), many DHABs have been discovered in different locations in the Red Sea (Backer and Schoell 1972), the Mediterranean Sea (Scientific Staff of Cruise Bannock 1984-12 1985), the Gulf of Mexico (Shokes et al. 1977) and the Black Sea (Aloisi et al. 2004; Figure 1). Despite the geology varies considerably for each specific case, in general, the majority of DHABs discovered so far originated by the re-dissolution of evaporitic deposits buried under layers of sediments and exposed to seawater because of tectonic activity (Cita 2006). This re-dissolution process generates the DHABs and a gradient of salinity, the Brine-Seawater Interface (BSI), at the boundary between the hypersaline water mass and seawater. Such salinity gradient is a halocline where the salt dissolution increases the water density determining a pycnocline. In Downloaded from https://academic.oup.com/femsec/advance-article-abstract/doi/10.1093/femsec/fiy085/4995905 by King Abdullah University of Science and Technology user on 20 May 2018 parallel to the gradient of salinity and density a chemocline occurs with gradients of the many chemical species that form redox couples capable of supporting different microbial metabolisms. The Red Sea hosts the largest number of documented DHABs (Figure 1) (Backer and Schoell 1972; Pautot et al. 1984). It has been proposed that during the Miocene period, the Red Sea became isolated from seawater influxes through the Bab El Mandeb Strait and the Gulf of Suez, possibly because of similar events that originated the Messinian Salinity Crisis in the Mediterranean Sea (Hsu, Stoffers and Ross 1978; Gargani, Moretti and Letouzey 2008; Garcia-Castellanos and Villasenor 2011). These events might have lead to the precipitation of several km of evaporites in the central trough of the Red Sea (Searle and Ross 1975). The Red Sea brines are categorized in two types depending on the postulated seismic origin and biogeochemical composition (Schmidt, Al-Farawati and Botz 2015). Type I, also named ―collapse-type‖ DHABs, includes Oceanographer Deep and Kebrit Deep. They present ranges - -1 -1 of high salinity (167-182 mg Cl l ), low pH (5.5-5.6) and, H2S (15-24 ml l ), mild warm temperatures (23.4-24.9°C) and low trace of heavy metals (Schmidt, Al-Farawati and Botz 2015). The geochemical characterization of type I DHABs indicates that their composition is not influenced by input of hydrothermal fluid and water/volcanic rock interaction, but rather by evaporite dissolution and sediment alteration. Type II, also named ―intrusion-/extrusion- related‖ DHABs, include the Conrad Deep, Shaban Deep and others located in the multi- deeps region of the Central Red Sea (Figure 1). Geochemically, these brines feature high concentrations of manganese (7-90 mg ml-1), and other metal ions, possibly due to hydrothermal input and subsurface water/volcanic rock interaction (Schmidt, Al-Farawati and Botz 2015). Many of the DHABs in the northern (Conrad, Shaban and Nereus) and central regions (Chain, Valdivia, Discovery, Shagara, Wando, Albatros, Atlantis II, Erba, Suakin and Port Sudan) of the Red Sea might have all been originated by the re-dissolution of evaporitic deposits subjected to the seismic events during the early seafloor spreading (Bonatti 1985). For instance, the influence of hydrothermal fluids is evidenced - and continues to occur - in Downloaded from https://academic.oup.com/femsec/advance-article-abstract/doi/10.1093/femsec/fiy085/4995905 by King Abdullah University of Science and Technology user on 20 May 2018 Atlantis II Deep and the interconnected Discovery Deep (Hartmann 1985; Hartmann et al. 1998; Swift, Bower and Schmitt 2012; Schardt 2015). The deepest brine pools described to date are located in the eastern Mediterranean Sea, all lying at depths greater than three km below the sea level (Figure 1; Cita 2006). Bannock, Discovery, Kryos, L‘Atalante, Medee, Thetis, Tyro and Urania sit on the Mediterranean Ridge accretionary wedge, which lies from west to east in the south of the island of Crete. Other brine pools have been reported in the Nile Deep Sea Fan off the Nile river delta (Huguen et al. 2009). Geological data, suggest that all the basins were produced by the dissolution of different layers of Messinian evaporites generated during the Messinian Salinity Crisis (Garcia-Castellanos and Villasenor, 2011), with subsequent fluid migration in confined depressions on the seafloor (Bortoluzzi et al. 2011). This explains the chemical differences in the composition of Mediterranean DHABs (van der Wielen et al. 2005). The brines in the Gulf of Mexico originated from the dissolution of evaporitic sheets, part of the Louann salt formation. Such a salt deposit was originally formed during the middle Jurassic (175-145 million years ago) and covered by sediments in the early Miocene. Gradual accumulation and differential loading of sediments caused the compression and generation of salt domes. Seismic events subsequently cracked the sediments leading to the dissolution of the evaporites (Cordes, Bergquist and Fisher 2009), originating several DHABs (Bouma and Bryant, 1994; Roberts et al. 2007). Some studies have shed some light on the microbial ecology of DHABs of the Gulf of Mexico, reviewed by Antunes, Ngugi and Stingl (2011) and Mapelli, Borin and Daffonchio (2012) and references therein. The Orca basin (Figure 1), a 400-km2 basin lying at about 2.25 km below sea level at the boundary between the Green Canyon and Walker Ridge protraction areas (Pilcher and Blumstein, 2007), was the first DHAB discovered in the Gulf of Mexico (Shokes et al. 1977; van Cappellen et al. 1998; Shah et al. 2013) and was followed by other smaller, low-salinity brines/mud volcanoes such as NR-1/GC233 and GB425 (Brooks et al. 1979; MacDonald et al. 1990), which have received attention in the last few years (Joye et al. 2009). Downloaded from https://academic.oup.com/femsec/advance-article-abstract/doi/10.1093/femsec/fiy085/4995905 by King Abdullah University of Science and Technology user on 20 May 2018 The Dvurechenskii mud volcano in the Black Sea (Aloisi et al. 2004; Figure 1) contains highly saline fluids enriched in Li, B, Ba, Sr, I and dissolved inorganic nitrogen. The analysis of the geochemical properties of the fluids indicated that they are not originated by the dissolution of evaporites, but from diagenetic processes (Aloisi et al. 2004). Unique features of DHABs Physical structure and productivity of DHABs Due to the high density (up to 1.35 g cm-3, as for the Discovery DHAB in the Mediterranean Sea; van der Wielen et al. 2005), and the high hydrostatic pressure, these brine pools hardly mix with the overlying deep seawater, and are often considered as lakes at the bottom of the sea.
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