Insights into the distribution and ecological role of members of the archaeal Phylum Bathyarchaeota. From the global to the local scale

Fillol Homs, Mireia
The Phylum Bathyarchaeota is currently one of the most studied uncultured archaeal phyla. Bathyarchaeota are phylogenetically diverse, globally ubiquitous and especially abundant in marine subsurface sediments. Despite their global significance, their ecological role is still unknown due to the lack of cultivated representatives and the paucity of available sequenced genomes. Besides, current distribution patterns provide few clues about their metabolic capabilities and physiological requirements. The current work tackled the problem by combining different phylogenetic and molecular techniques to shed light on the main environmental drivers that affect the distribution patterns of Bathyarchaeota at a global and regional scale. Our results showed that the phylum Bathyarchaeota went across various saline–freshwater transitions during its evolution that caused diversification events that resulted in subgroups specifically adapted to marine and saline habitats. Besides, our approach provided a robust ecological framework in which Bathyarchaeota appear as a core generalist group in the sediment realm, sharing their key role with other uncultured archaeal lineages such as the Thermoplasmata. At a regional scale, a molecular survey carried out in different stratified lakes of the Banyoles Karstic System provided evidences that Bathyarchaeota are a common component of archaeal assemblages thriving in both euxinic water compartments and sediments. Multivariate analyses identified sulfide and dissolved organic carbon as main environmental variables that explain the distribution of Bathyarchaeota subgroups between the planktonic and sedimentary habitats. In the latter, Bathyarchaeota were particularly prevalent in biofilms developed on leaf litter settled in sediments of Lake Cisó, that provided a natural enrichment where to better characterize their habitat segregation, phylogenetic diversity and membrane lipid composition. The application of complementary molecular tools such as massive sequencing of 16S rRNA gene and lipidomics revealed that biofilms were almost solely composed of subgroup Bathyarchaeota-6 and possessed a characteristic, and hitherto unknown, profile of isomeric isoprenoid tetraether lipids GDGT-1, -2 and -3. Altogether, our study recognised Bathyarchaeota as key players in marine and freshwater sediments at both global and regional scales. We also identified the main environmental drivers behind their group diversification and current subgroup segregation, and stablished the co-occurrence and putative synergy between members of the Phylum Bathyarchaeota and the class Thermoplasmata. Besides, our work provides new molecular tools to better address ecological studies focused on the Bathyarchaeota and make an important step forward to finally find a specific lipid biomarker for this widespread and diverse archaeal lineage. ​
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