Halorhabdus tiamatea: Complete genome sequencing and proteomics identify the first cultivated euryarchaeon from a deep-sea anoxic brine lake as polysaccharide degrader. Halorhabdus tiamatea SARL4B

Background: Members of the euryarchaeal genus Halorhabus have been found in various hypersaline habitats, but so far are represented by only two isolates: H. utahensis AX-2T, a facultative anaerobe from the shallow Great Salt Lake of Utah, and H. tiamatea SARL4BT, an almost obligate anaerobe from the Shaban deep-sea hypersaline anoxic lake in the Red Sea, whose ecology is not well understood. Results: Here we present the complete genome of H. tiamatea SARL4BT and elucidate its niche adaptations. H. tiamatea SARL4BT excels as a polysaccharide-degrader as it constitutes the archaeon with the as yet highest number of glycoside hydrolases. Even though H. tiamatea SARL4BT inhabits a temperate, light-less, anoxic environment, its genome encodes genes usually found in hyperthermophiles, light-dependent enzymes such as bacteriorhodopsin, and a complete aerobic redox chain. Proteome analyses showed a pronounced stress response to oxygen, but simultaneously indicated possible respiration, and furthermore demonstrated relevance of the glycoside hydrolases. We could furthermore identify a closely related Halorhabus member in the Mediterranean deep-sea halophilic anoxic lake Medee by metagenomics and fluorescence in situ hybridization. Conclusions: Comparative genomics with H. utahensis AX-2T suggests that H. tiamatea SARL4BT evolved from a thermophile inhabiting an oxic habitat in the photic zone. H. tiamatea SARL4BT seems to have specialized on the degradation of recalcitrant algae and seagrass hemicelluloses that reach the deep-sea. Identification of a closely related Halorhabus member in the Mediterranean supports genetic drift among seemingly isolated hypersaline habitats and thus might explain why Halorhabdi have been found in such habitats worldwide.