Natronogracilivirga saccharolytica gen. nov., sp. nov. and Cyclonatronum proteinivorum gen. nov., sp. nov., haloalkaliphilic organotrophic bacteroidetes from hypersaline soda lakes forming a new family Cyclonatronaceae fam. nov. in the order Balneolales

Soda lakes are a special type of inland salt lakes located in the semi-arid or arid climatic zones and characterized by high (≥9.0) pH caused by the presence of carbonate and bicarbonate ions and often by high mineralization resulting in extremely high alkaline buffering capacity. Intensive study of soda lakes performed during the last 30 years resulted in understanding that despite extreme parameters they characterized by high level of biomass production and active biogeochemical carbon, nitrogen, sulfur and iron cycling caused by the activity of functionally and phylogenetically diverse microorganisms, mainly represented by prokaryotes (last reviewed: (Antony et al., 2013, Sorokin, 2017, Sorokin et al., 2015, Sorokin et al., 2014), (Gracheva et al., 2017, Zavarzina et al., 2006, Zavarzina et al., 2020, Zhilina et al., 2015). Currently, a picture of trophic interactions in the haloalkaliphilic environments is fairly complete and the main actors and their trophic interactions are discovered. Particularly important role in mineralization of autochthonous organic matter is played by organoheterotrophic microorganisms, which include both aerobic and anaerobic bacteria and archaea.

The dominant primary producers of organic matter in Siberian saline soda lakes belong to haloalkaliphilic oxygenic benthic filamentous cyanobacteria of the genera Nodosilinea and Geitlerinema (Samylina et al., 2014). Their cell wall is rich in proteins and polysaccharides, and among all others this capacity is most characteristic of the filamentous diazotrophic species (Vargas et al., 1998). The aerobic haloalkaliphilic protein-utilizing strain OmegaT (Balneolales), that consistently developed as a heterotrophic satellite in several enrichment cultures of haloalkaliphilic filamentous cyanobacteria obtained from a soda lake in southwestern Siberia has previously been described as Candidatus Cyclonatronum proteinivorum with the focus on its metabolic capacities, revealed by cultivation and genomic analysis (Sorokin et al., 2018). Here we add some additional phenotypic and chemotaxonomy characteristics for this species to finalize its formal taxonomy description.

Carbohydrate-fermenting anaerobes are an essential primary step in the mineralization of organic matter by anaerobic microbial communities. In soda lakes, several alkaliphilic carbohydrate-utilizing anaerobic organotrophs were described (Garnova et al., 2004, Garnova et al., 2003, Hoover et al., 2003, Pikuta et al., 2009, Vishnuvardhan Reddy et al., 2013, Zavarzina et al., 2009, Zhilina et al., 2004, Zhilina et al., 2001, Zhilina et al., 2001, Zhilina et al., 1996). Some of them are capable of hydrolyzing partially soluble and insoluble polysaccharides (Sorokin et al., 2011, Sorokin et al., 2012, Zhilina et al., 2005, Zhilina et al., 2004). The others incapable of hydrolyzing polymeric substrates frequently act as satellites of polysaccharide-degrading co-habitants or participate in cell degradation of chemotrophic prokaryotes consuming mono- and oligomeric depolymerization products.

In this work we describe an alkaliphilic, anaerobic carbohydrate-fermenting bacterium, strain Z-1702T, as a representative of the novel genus and species Natronogracilivirga saccharolityca gen. nov., sp. nov.. Together with the previously described proteolytic Isachenkonia alkalipeptolitica (Zavarzina et al., 2020) N. saccharolityca acted as an oligo-heterotrophic satellite in lithoautotrophic iron-reducing culture. Furthermore, a taxomic description of Ca. Cyclonatronum proteinivorum, strain OmegaT (Sorokin et al., 2018) is provided. N. saccharolityca and its closest relative Ca. Cyclonatronum proteinivorum are forming a deep-branching family-level lineage within the order Balneolales for which the name Cyclonatronaceae fam. nov. is proposed.

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