Stratified prokaryote network in the oxic–anoxic transition of a deep-sea halocline

Abstract

The chemical composition of the Bannock basin has been studied in some detail 1,2 . We recently showed that unusual microbial populations, including a new division of Archaea (MSBL1) 3 , inhabit the NaCl-rich hypersaline brine. High salinities tend to reduce biodiversity 4 , but when brines come into contact with fresher water the natural haloclines formed frequently contain gradients of other chemicals, including permutations of electron donors and acceptors, that may enhance microbial diversity, activity and biogeochemical cycling 5,6 . Here we report a 2.5-mthick chemocline with a steep NaCl gradient at 3.3 km within the water column betweeen Bannock anoxic hypersaline brine 7 and overlying sea water. The chemocline supports some of the most biomass-rich and active microbial communities in the deep sea, dominated by Bacteria rather than Archaea, and including four major new divisions of Bacteria. Significantly higher metabolic activities were measured in the chemocline than in the overlying sea water and underlying brine; functional analyses indicate that a range of biological processes is likely to occur in the chemocline. Many prokaryotic taxa, including the phylogenetically new groups, were confined to defined salinities, and collectively formed a diverse, sharply stratified, deep-sea ecosystem with sufficient biomass to potentially contribute to organic geological deposits.High-precision sampling was conducted during cruises of the research vessel Urania equipped with the Modus-Scipack system (http://www.geo.unimib.it/BioDeep/Project.html; Fig. 1a). The vehicle Modus, connected by cable to the research vessel, held a second instrument, the Scipack, with a 10-m data transmission cable. The Scipack, consisting of a Rosette sampler equipped with a CTD (conductivity-temperature-depth probe) and a series of Niskin bottles, was connected to the Modus through the Sciskid, a module equipped with a pressure sensor for recording the pressure at which the Niskin bottles were closed (Fig. 1c). A camera on the Modus could provide an image of the Scipack entering the brine lake (Fig. 1b, and Supplementary Fig. S1). Immediately after sampling, the Modus-Scipack was raised, the Niskin bottles were retrieved and their contents were carefully fractionated on board ship by slowly recovering 0.5-litre, 1-litre or 2-litre fractions from the bottom tap. These were then immediately analysed for salinity (Fig. 1d). The reconstructed interface salinity profile was strongly positively correlated (r ¼ 0.98, P , 0.001) with the CTD conductivity profile recorded in independent non-sampling casts (Fig. 2d), indicating that little or no mixing had occurred.The interface halocline was about 2.5 m deep, in agreement with previous estimates that employed alternative sampling strategies 1 . Although biomass values fluctuated along the halocline, there were significantly greater numbers of microbial cells in the interface (about 10 6 cells ml 21 ) than in either the deep sea water or the underlying hypersaline brine, both of which had about...

Inter-comparison of the potentially active prokaryotic communities in the halocline sediments of Mediterranean deep-sea hypersaline basins

“…Daffonchio et al 2006;Yakimov et al 2007a,b;La Cono et al 2011) and unicellular eukaryotes (e.g. Edgcomb et al 2009;Pachiadaki et al 2014) found in the seawater--brine interfaces and the brines of several of these systems.…”

“…Indeed, microbial life from all three domains has been shown to occur in such aquatic systems (e.g. van der Wielen et al 2005;Daffonchio et al 2006;Alexander et al 2009;Borin et al 2009;Yakimov et al 2007a). While new cell morphologies and ecophysiological traits have been assigned to some of these microorganisms, only recently a more specific picture of the metabolic activities of DHAB microorganisms has started to emerge, e.g.…”

Unveiling microbial activities along the halocline of Thetis, a deep-sea hypersaline anoxic basin

“…This is the first time that evidence for nitrogen fixation activity in a DHAB habitat is reported. In ammonium-rich environments such as the DHAB interfaces and brines (Daffonchio et al, 2006), dinitrogen fixation is expected to be inhibited (Madigan et al, 2008), but some organisms are capable of maintaining high N 2 fixation rates in the presence of a high level of ammonium. This was observed in isolates (Okoronkwo et al, 1989) and in natural populations from deep anoxic waters of the Baltic Sea (Farnelid et al, 2013).…”

“…Studies of Discovery, L'Atalante, Urania, Thetis and Bannock basins revealed that DHAB interfaces harbor abundant and diverse microbial communities that include numerous novel candidate divisions that are more productive than most pelagic marine systems (see, for example, Sass et al, 2001;Van Der Wielen et al, 2005;Yakimov et al, 2007;Edgcomb et al, 2009;Stock et al, 2012). Functional analyses of these communities based on PCR amplification of key functional genes as well as activity measurements revealed sulfur cycling and methanogenesis to be dominant prokaryotic metabolic processes supporting life in DHABs and contributing to observed elevated biomass in DHAB haloclines (Daffonchio et al, 2006;Yakimov et al, 2007;Borin et al, 2009). Recent advances in RNA isolation, amplification and high-throughput sequencing make it possible to acquire millions of sequences of transcribed genes from microbial communities.…”

Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean Sea

“…They were formed 5000-40 000 years ago by dissolution of ancient subterranean salt deposits (Messinian evaporites) exposed to seawater by tectonic shifts and the downward flow of the dense brines into local abyssal depressions, followed by progressive development of anoxia in the brine lakes thereby formed (Fusi et al, 1996;Wallmann et al, 1997). Recent studies of DHALs revealed the existence of new microbial lineages flourishing within these harsh environments (Ferrer et al, 2005;van der Wielen et al, 2005;Daffonchio et al, 2006;Hallsworth et al, 2007;Yakimov et al, 2007).…”