Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the eastern Mediterranean Sea

Abstract

Non-standard abbreviations:DHAB -deep hypersaline anoxic basin UMA -uncultured marine alveolate clade 2 AbstractEnvironmental factors restrict the distribution of microbial eukaryotes but the exact boundaries for eukaryotic life are not known. Here we examine protistan communities at the extremes of salinity and osmotic pressure, and report rich assemblages inhabiting Bannock and Discovery, two deep-sea superhaline anoxic basins in the Mediterranean. Using a rRNA-based approach, we detected 1538 protistan rRNA gene sequences from water samples with total salinity ranging from 39 g/kg to 280 g/Kg, and obtained evidence that this DNA was endogenous to the extreme habitats sampled. Statistical analyses indicate that the discovered phylotypes represent only a fraction of species actually inhabiting both the brine and the brine-seawater interface, with as much as 82% of the actual richness missed by our survey. Jaccard indices (e.g., for a comparison of community membership) suggest that the brine/interface protistan communities are unique to Bannock and Discovery basins, and share little (0.8-2.8%) in species composition with overlying waters with typical marine salinity and oxygen tension. The protistan communities from the basins' brine and brine/seawater interface appear to be particularly enriched with dinoflagellates, ciliates and other alveolates, as well as fungi, and are conspicuously poor in stramenopiles. The uniqueness and diversity of brine and brine-interface protistan communities make them promising targets for protistan discovery.

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

“…Euglenozoan, jakobid, rhizarian and choanoflagellate signatures were only detected in the UI, indicating a decrease in diversity in the anoxic and more hypersaline layer. Other studies have found ciliates to dominate the eukaryotic microbial community in upper DHAB haloclines (Alexander et al, 2009;Edgcomb et al, 2009), but we observed a decrease in the relative abundance of ciliate rRNA as environmental conditions become more challenging in the LI, where Fungi appear equally abundant.…”

“…Based on SSU rRNA gene transcripts recovered within our metatranscriptome libraries, the eukaryotic community appears to be dominated by ciliates and dinoflagellates in the UI, and by ciliates and fungi in the LI (Figure 2). Previous studies of DHABs, including Thetis, based on SSU rRNA and microscopic observations have detected heterotrophic protists (particularly ciliates, dinoflagellates and fungi) in up to 36% salinity (see, for example, Alexander et al, 2009;Edgcomb et al, 2009;Stock et al, 2012). Phagotrophic protists are known to be successful along pelagic oxyclines where prokaryotes are abundant (see, for example, Behnke et al, 2006;Edgcomb et al, 2011a) and hence it follows that they are also successful within these haloclines.…”

“…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).…”

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.…”

Large-scale patterns in biodiversity of microbial eukaryotes from the abyssal sea floor

“…Environmental molecular surveys have revolutionized our understanding of microbial systems (6). Phylogenetic surveys also have been applied successfully to study the community composition of eukaryotic microbes at several deep-sea sites (7)(8)(9)(10)(11)(12)(13)(14)(15)(16); however, to date, no study has addressed the phylogenetic diversity of eukaryotic microbial life of one of the largest habitats, covering over half of the Earth's surface: the abyssal plains.…”