Sulfur Respiration in a Group of Facultatively Anaerobic Natronoarchaea Ubiquitous in Hypersaline Soda Lakes.

Dimitry Y Sorokin,Michail M Yakimov,Violetta La Cono,Stepan V Toshchakov,Sergio Ciordia,Peter N Golyshin,Enzo Messina,Maria C Mena,Manuel Ferrer

doi:10.3389/fmicb.2018.02359

Abstract

The ubiquity of strictly anaerobic sulfur-respiring haloarchaea in hypersaline systems with circumneutral pH has shaken a traditional concept of this group as predominantly aerobic heterotrophs. Here, we demonstrated that this functional group of haloarchaea also has its representatives in hypersaline alkaline lakes. Sediments from various hypersaline soda lakes showed high activity of sulfur reduction only partially inhibited by antibiotics. Eight pure cultures of sulfur-reducing natronoarchaea were isolated from such sediments using formate and butyrate as electron donors and sulfur as an electron acceptor. Unlike strict anaerobic haloarchaea, these novel sulfur-reducing natronoarchaea are facultative anaerobes, whose metabolic capabilities were inferred from cultivation experiments and genomic/proteomic reconstruction. While sharing many physiological traits with strict anaerobic haloarchaea, following metabolic distinctions make these new organisms be successful in both anoxic and aerobic habitats: the recruiting of heme-copper quinol oxidases as terminal electron sink in aerobic respiratory chain and the utilization of formate, hydrogen or short-chain fatty acids as electron donors during anaerobic growth with elemental sulfur. Obtained results significantly advance the emerging concept of halo(natrono)archaea as important players in the anaerobic sulfur and carbon cycling in various salt-saturated habitats.

Highlights

Halophilic archaea representing the class Halobacteria within the phylum Euryarchaeota are predominant inhabitants in salt-saturated environments
To assess potential sulfur-reducing activity, 1:1 slurries were prepared from surface sediments (5–10 cm deep) and near bottom brines (1:1, vol/vol) from two soda lakes in Kulunda Steppe (Altai, Russia) taken in 2011: a moderately saline Cock soda lake and a hypersaline Bitter-1 lake. 10 ml slurries were dispensed into 23 ml serum bottles and 10 mg powdered sulfur and various e-donors at 2–5 mM were added
The salinity profiling of the potential formate-dependent sulfurreducing activity in sediments from the two different soda lakes showed a profound difference: while the activity dropped sharply after salinity increase above 2 M total Na+ in the moderately saline Cock Soda Lake, it reached maximum at saturated sodium carbonate concentrations in the hypersaline Bitter-1 lake (Figure 1A) indicating a possible involvement of the natronoarchaea in this process in the latter lake

Summary

Introduction

Halophilic archaea representing the class Halobacteria within the phylum Euryarchaeota are predominant inhabitants in salt-saturated environments They are surprisingly diverse in their ecophysiology in relation to the carbon metabolism and to the type of respiration. The second group, described as Halodesulfurarchaeum formicicum (HDA), represents the first example of lithoheterotrophy in haloarchaea These organisms can use formate or H2 as the electron donor and elemental sulfur, thiosulfate or DMSO as the electron acceptor (Sorokin et al, 2017b). The discovery of these two ubiquitous groups of strictly anaerobic sulfur-respiring haloarchaea living in anoxic sediments of hypersaline lakes showed that the existing concept of the haloarchaeal physiology requires revision

Methods

Results

Conclusion