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Halo(natrono)archaea isolated from hypersaline lakes utilize cellulose and chitin as growth substrates.

ABSTRACT: Until recently, extremely halophilic euryarchaeota were considered mostly as aerobic heterotrophs utilizing simple organic compounds as growth substrates. Almost nothing is known on the ability of these prokaryotes to utilize complex polysaccharides, such as cellulose, xylan, and chitin. Although few haloarchaeal cellulases and chitinases were recently characterized, the analysis of currently available haloarchaeal genomes deciphered numerous genes-encoding glycosidases of various families including endoglucanases and chitinases. However, all these haloarchaea were isolated and cultivated on simple substrates and their ability to grow on polysaccharides in situ or in vitro is unknown. This study examines several halo(natrono)archaeal strains from geographically distant hypersaline lakes for the ability to grow on insoluble polymers as a sole growth substrate in salt-saturated mineral media. Some of them belonged to known taxa, while other represented novel phylogenetic lineages within the class Halobacteria. All isolates produced extracellular extremely salt-tolerant cellulases or chitinases, either cell-free or cell-bound. Obtained results demonstrate a presence of diverse populations of haloarchaeal cellulo/chitinotrophs in hypersaline habitats indicating that euryarchaea participate in aerobic mineralization of recalcitrant organic polymers in salt-saturated environments.

SUBMITTER: Sorokin DY

PROVIDER: S-EPMC4569967 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Halo(natrono)archaea isolated from hypersaline lakes utilize cellulose and chitin as growth substrates.

Sorokin Dimitry Y DY Toshchakov Stepan V SV Kolganova Tatyana V TV Kublanov Ilya V IV

Frontiers in microbiology 20150915

Until recently, extremely halophilic euryarchaeota were considered mostly as aerobic heterotrophs utilizing simple organic compounds as growth substrates. Almost nothing is known on the ability of these prokaryotes to utilize complex polysaccharides, such as cellulose, xylan, and chitin. Although few haloarchaeal cellulases and chitinases were recently characterized, the analysis of currently available haloarchaeal genomes deciphered numerous genes-encoding glycosidases of various families inclu ...[more]

PMID: 26441877

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Project description:We analyzed the polar membrane lipids of 13 strains of halo(alkali)philic euryarchaea from hypersaline lakes. Nine belong to the class Halobacteria, representing two functional groups: aerobic polysaccharide utilizers and sulfur-respiring anaerobes. The other four strains represent halo(alkali)philic methanogens from the class Methanomicrobia and a recently discovered class Methanonatronarchaeia. A wide range of polar lipids were detected across the 13 strains including dialkyl glycerol diethers (archaeols), membrane-spanning glycerol tetraethers and diether-based cardiolipins. The archaeols contained a range of core lipid structures, including combinations of C20 and C25 isoprenoidal alkyl chains, unsaturations, and hydroxy moieties. Several diether lipids were novel, including: (a) a phosphatidylglycerolhexose (PG-Gly) headgroup, (b) a N,N,N-trimethyl aminopentanetetrol (APT)-like lipid with a methoxy group in place of a hydroxy group on the pentanetetrol, (c) a series of polar lipids with a headgroup with elemental composition of either C12H25NO13S or C12H25NO16S2, and (d) novel cardiolipins containing a putative phosphatidylglycerolphosphate glycerophosphate (PGPGP) polar moiety. We found that the lipid distribution of the 13 strains could be generally separated into two groups, the methanogens (group) and the Halobacteria (class) based on the presence of specific core lipids. Within the methanogens, adaption to a high or more moderate salt concentration resulted in different ratios of glycerol dialkyl glycerol tetraethers (GDGTs) to archaeol. The methanogen Methanosalsum natronophilum AME2T had the most complex diether lipid composition of any of the 13 strains, including hydroxy archaeol and macrocyclic archaeol which we surmise is an order-specific membrane adaption. The zwitterionic headgroups APT and APT-Me were detected only in the Methanomicrobiales member Methanocalculus alkaliphilus AMF2T which also contained the highest level of unsaturated lipids. Only alkaliphilic members of the Natrialbales order contained PGPGP cardiolipins and the PG-Gly headgroup. The four analyzed neutrophilic members of the Halobacteria were characterized by the presence of sulfur-containing headgroups and glycolipids. The presence of cardiolipins with one or more i-C25 alkyl chains, generally termed extended archaeol (EXT-AR), in one of the Methanonatronarchaeia strains was unexpected as only one other order of methanogenic archaea has been reported to produce EXT-AR. We examined this further by looking into the genomic potential of various archaea to produce EXT-AR.

Project description:Two groups of alkaliphilic haloarchaea from hypersaline alkaline lakes in Central Asia, Egypt and North America were enriched and isolated in pure culture using chitin as growth substrate. These cultures, termed AArcht, were divided into two groups: group 1 which includes eleven isolates from highly alkaline soda lakes and group 2 which contains a single isolate obtained from the alkaline hypersaline Searles Lake. The colonies of chitin-utilizing natronoarchaea were red-pigmented and surrounded by large zones of chitin hydrolysis. The free cells of both groups were mostly flat nonmotile rods, while the cells that attached to chitin or formed colonies on chitin plates were mostly coccoid. The isolates are obligate aerobic saccharolytic archaea utilizing chitin and chitosane (less actively) as the only sugar polymers as well as a few hexoses as their carbon and energy source. Both groups are extremely halophilic, growing optimally at 3.5-4M total Na+, but they differ in their pH profiles: the main group 1 isolates are obligately alkaliphilic, while the single group 2 strain (AArcht-SlT) is alkalitolerant. The core archaeal lipids in both groups are dominated by C20-C20 and C20-C25 dialkyl glycerol ethers (DGE) in approximately equal proportion. Phylogenetic analysis indicated that the isolates form an independent genus-level lineage within the family Natrialbaceae with 3 species-level subgroups. The available genomes of the closest cultured relatives of the AArcht strains, belonging to the genera Natrialba and Halopiger, do not encode any chitinase-related genes. On the basis of their unique phenotypic properties and distinct phylogeny, we suggest that the obligate alkaliphilic AArcht isolates (group 1) with an identical phenotype are classified into a new genus and species Natrarchaeobius chitinivorans gen. nov., sp. nov., with strain AArcht4T as the type strain (JCM 32476T=UNIQEM U966T), while the facultatively alkaliphilic strain AArcht-SlT (group 2) - as a new species Natrarchaeobius halalkaliphilus sp. nov. (JCM 32477T=UNIQEM U969T).

Dataset Information

Halo(natrono)archaea isolated from hypersaline lakes utilize cellulose and chitin as growth substrates.

Publications

Halo(natrono)archaea isolated from hypersaline lakes utilize cellulose and chitin as growth substrates.

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