Microbial ecology of an Antarctic hypersaline lake: genomic assessment of ecophysiology among dominant haloarchaea

Williams, Timothy J.; Allen, Michelle A.; DeMaere, Matthew Z.; Kyrpides, Nikos C.; Tringe, Susannah G.; Woyke, Tanja; Cavicchioli, Ricardo

doi:10.1038/ismej.2014.18

Cited by 51 publications

(79 citation statements)

References 64 publications

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“…Statistical analyses (ANOSIM and NMDS) were performed to assess the relationship of taxon and cellular function with lake depth and size fraction. Below, we present findings that verify or refute previous inferences (17,19) and advance our overall understanding of Deep Lake ecology. Additional results are provided in the supplemental material.…”

Section: Resultssupporting

confidence: 66%

“…The mass spectrometry data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository under project name Metaproteome, Deep Lake, Antarctica, with project accession number PXD001436 (10). Analytical approaches were based on methods described previously for studying Antarctic lake ecosystems (7)(8)(9)(10)(17)(18)(19). Briefly, a composite database comprised of assemblies of Deep Lake metagenome data and the genome sequences of the Deep Lake haloarchaea Halohasta litchfieldiae, undescribed genus strain DL31, Halorubrum lacusprofundi, and Halobacterium sp.…”

Section: Methodsmentioning

confidence: 99%

“…In particular, "variants" of cell surface proteins (e.g., main S-layer protein) were linked to providing a mechanism of infection evasion by preventing virus adsorption (10). With metaproteomic methods developed for this Antarctic lake, the first for any hypersaline environment (10), in this study, we sought to describe proteins that pertain to pathways and cellular processes present in these haloarchaea, test the validity of the previous genome-based predictions (17,19), and establish how the main genera and strains coexist and utilize available natural resources. By utilizing biomass captured on 3.0-, 0.8-, and 0.1-m filters from 0-, 5-, 13-, 24-, and 36-m depths of the lake, this study was able to test the hypothesis that functional distinctions in the community occurred primarily between genera and between strains and not between communities or individuals separated by lake depth or filter size.…”

mentioning

confidence: 99%

“…litchfieldiae was inferred to possess swimming motility with a saccharolytic metabolism that included a preference for glycerol utilization, DL31 was inferred to target mainly peptides and amino acids, and Hrr. lacusprofundi was inferred to be less specialized in the nutrients that it targets (19). Strain-level phylotypes were also identified by using fragment recruitment of metagenome data to the closed genomes of the isolates, single-nucleotide polymorphism (SNP) analyses, and GC/read-depth profiling of the de novo assembly of metagenome data (17).…”

mentioning

confidence: 99%

“…strain DL1, which represents a minor fraction (ϳ0.3%) of the lake community, were predicted from their genome sequences (19). Hht.…”

mentioning

confidence: 99%

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Ecophysiological Distinctions of Haloarchaea from a Hypersaline Antarctic Lake as Determined by Metaproteomics

Tschitschko

Williams

Allen

et al. 2016

Appl Environ Microbiol

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Deep Lake in the Vestfold Hills is hypersaline and the coldest system in Antarctica known to support microbial growth (temperatures as low as ؊20°C). It represents a strong experimental model because the lake supports a low-complexity community of haloarchaea, with the three most abundant species totaling ϳ72%. Moreover, the dominant haloarchaea are cultivatable, and their genomes are sequenced. Here we use metaproteomics linked to metagenome data and the genome sequences of the isolates to characterize the main pathways, trophic strategies, and interactions associated with resource utilization. The dominance of the most abundant member, Halohasta litchfieldiae, appears to be predicated on competitive utilization of substrates (e.g., starch, glycerol, and dihydroxyacetone) produced by Dunaliella, the lake's primary producer, while also possessing diverse mechanisms for acquiring nitrogen and phosphorus. The second most abundant member, strain DL31, is proficient in degrading complex proteinaceous matter. Hht. litchfieldiae and DL31 are inferred to release labile substrates that are utilized by Halorubrum lacusprofundi, the third most abundant haloarchaeon in Deep Lake. The study also linked genome variation to specific protein variants or distinct genetic capacities, thereby identifying strain-level variation indicative of specialization. Overall, metaproteomics revealed that rather than functional differences occurring at different lake depths or through size partitioning, the main lake genera possess major trophic distinctions, and phylotypes (e.g., strains of Hht. litchfieldiae) exhibit a more subtle level of specialization. This study highlights the extent to which the lake supports a relatively uniform distribution of taxa that collectively possess the genetic capacity to effectively exploit available nutrients throughout the lake. IMPORTANCELife on Earth has evolved to colonize a broad range of temperatures, but most of the biosphere (ϳ85%) exists at low temperatures (<5°C). By performing unique roles in biogeochemical cycles, environmental microorganisms perform functions that are critical for the rest of life on Earth to survive. Cold environments therefore make a particularly important contribution to maintaining healthy, stable ecosystems. Here we describe the main physiological traits of the dominant microorganisms that inhabit Deep Lake in Antarctica, the coldest aquatic environment known to support life. The hypersaline system enables the growth of halophilic members of the Archaea: haloarchaea. By analyzing proteins of samples collected from the water column, we determined the functions that the haloarchaea were likely to perform. This study showed that the dominant haloarchaea possessed distinct lifestyles yet formed a uniform community throughout the lake that was collectively adept at using available light energy and diverse organic substrates for growth.

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Section: Resultssupporting

confidence: 66%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

“…strain DL1, which represents a minor fraction (ϳ0.3%) of the lake community, were predicted from their genome sequences (19). Hht.…”

mentioning

confidence: 99%

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Ecophysiological Distinctions of Haloarchaea from a Hypersaline Antarctic Lake as Determined by Metaproteomics

Tschitschko

Williams

Allen

et al. 2016

Appl Environ Microbiol

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Halobacterium

Oren¹,

Ventosa²

2017

Bergey's Manual of Systematics of Archaea and Bacteria

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Ha.lo.bac.te'ri.um. Gr. n. hals, halos salt; L. neut. n. bacterium , a small rod; N.L. neut. n. Halobacterium salt (‐requiring) bacterium. Euryarchaeota / Halobacteria / Halobacteriales / Halobacteriaceae / Halobacterium The genus Halobacterium , classified within the family Halobacteriaceae , order Halobacteriales in the class Halobacteria , consists of motile rod‐shaped cells that form colonies pigmented red to pink by bacterioruberin carotenoids. Retinal pigments such as bacteriorhodopsin and halorhodopsin may also be present. All species are extremely halophilic, and some isolates produce gas vesicles. They are aerobes, catalase positive; the oxidase reaction is variable. Some strains can grow in the absence of molecular oxygen by anaerobic respiration with nitrate or dimethylsulfoxide as the electron acceptor, and most isolates grow anaerobically by fermentation of arginine. Most species have complex growth requirements, and sugars are poorly metabolized. Polar lipids are diphytanyl diether derivatives of phosphatidylglycerol, the methyl ester of phosphatidylglycerol phosphate, phosphatidylglycerol sulfate, sulfated triglycosyl‐ and tetraglycosyl diether lipids, and other glycolipids. Currently, the genus consists of four species. Isolates have been recovered from salted fish, salted hides, marine salterns, natural salt lakes, and rock salt. DNA G + C content (mol%) : 54.3–71.2. Type species : Halobacterium salinarum .

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Halorubrum

Oren¹

2018

Bergey's Manual of Systematics of Archaea and Bacteria

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Ha.lo.ru'brum . Gr. n. hals , halos , salt; L. neut. adj. rubrum , red; N.L. neut. n. Halorubrum salt (‐requiring) and red. Euryarchaeota / Halobacteria / Haloferacales / Halorubraceae / Halorubrum With 37 species, Halorubrum (family Halorubraceae , order Haloferacales ) is the largest genus within the class Halobacteria . Cells of Halorubrum species are rod shaped or pleomorphic under optimal growth conditions and stain Gram‐negative. Some species are motile. Colonies are generally red‐orange due to the presence of bacterioruberin carotenoids, but some species are almost colorless; retinal pigments can also be present. Some strains produce gas vesicles. Halorubrum species are extremely halophilic, with growth occurring in media containing 1.0–5.2 M NaCl; the optimum magnesium concentration varies between 0.005 and 0.6 M. Cells lyse in distilled water. The genus contains both neutrophilic and alkaliphilic species. All are aerobic chemoorganotrophs; anaerobic growth of some species was reported in the presence of nitrate or arginine. Some species grow on single carbon sources. Most species use sugars, some with the production of acids. The major polar lipids are C 20 C 20 and sometimes C 20 C 25 glycerol diether derivatives of phosphatidylglycerol, phosphatidylglycerol phosphate methyl ester, phosphatidylglycerol sulfate (in most species), and a sulfated glucosyl mannosyl diether, for some species identified as S‐DGD‐3. Alkaliphilic species lack glycolipids. The DNA G + C content is between 60.2 and 71.2 mol%. Halorubrum species have been isolated from marine salterns, salt lakes, soda lakes, saline soils, rock salt, salted foods, and other hypersaline environments. The type species is Halorubrum saccharovorum . Later homotypic synonym: Halorubrobacterium Kamekura and Dyall‐Smith 1996, 625 VP (Effective publication: Kamekura and Dyall‐Smith 1995, 345). DNA G + C content (mol%) : 60.2–71.2. Type species : Halorubrum saccharovorum (Tomlinson and Hochstein 1976) McGenity and Grant 1996, 362 VP (Effective publication: McGenity and Grant 1995, 241) ( Halobacterium saccharovorum Tomlinson and Hochstein 1977, 306; Halorubrobacterium saccharovorum (Tomlinson and Hochstein 1976) Kamekura and Dyall‐Smith 1996, 625).

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Microbial ecology of an Antarctic hypersaline lake: genomic assessment of ecophysiology among dominant haloarchaea

Cited by 51 publications

References 64 publications

Ecophysiological Distinctions of Haloarchaea from a Hypersaline Antarctic Lake as Determined by Metaproteomics

Ecophysiological Distinctions of Haloarchaea from a Hypersaline Antarctic Lake as Determined by Metaproteomics

Halobacterium

Halorubrum

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