The genome of Salinibacter ruber : Convergence and gene exchange among hyperhalophilic bacteria and archaea

Abstract

Saturated thalassic brines are among the most physically demanding habitats on Earth: few microbes survive in them. Salinibacter ruber is among these organisms and has been found repeatedly in significant numbers in climax saltern crystallizer communities. The phenotype of this bacterium is remarkably similar to that of the hyperhalophilic Archaea (Haloarchaea). The genome sequence suggests that this resemblance has arisen through convergence at the physiological level (different genes producing similar overall phenotype) and the molecular level (independent mutations yielding similar sequences or structures). Several genes and gene clusters also derive by lateral transfer from (or may have been laterally transferred to) haloarchaea. S. ruber encodes four rhodopsins. One resembles bacterial proteorhodopsins and three are of the haloarchaeal type, previously uncharacterized in a bacterial genome. The impact of these modular adaptive elements on the cell biology and ecology of S. ruber is substantial, affecting salt adaptation, bioenergetics, and photobiology.halophile ͉ lateral gene transfer ͉ convergence ͉ prokaryotic evolution ͉ rhodopsins U ntil recently, halophilic archaea (haloarchaea) were thought to be the only cells capable of thriving in saltern crystallizers. These impoundments contain Ϸ37% NaCl, at the limits of tolerance for this environmental factor. Further concentration of thalassic (seawater-derived) hypersaline water leads to precipitation of magnesium salts and sterility. Fluorescent in situ hybridization indicates that one crystallizer morphotype, well defined large rods, corresponds to a bacterium of the Cytophaga cluster (1), within the Bacteroides͞Chlorobi group. This organism represents 10-20% of the cells in climax crystallizer communities (spring and summer in temperate latitudes). Representative strains (as defined by 16S rRNA sequences) have been isolated from the same environment and described as the previously uncharacterized genus and species Salinibacter ruber (2).The closest cultivated relative of S. ruber (henceforth Salinibacter) is Rhodothermus marinus (89% 16S rRNA sequence similarity), a slightly halophilic thermophile isolated from marine hot springs (2). Salinibacter displays many remarkable similarities to haloarchaea, one being a very high concentration of potassium in the cytoplasm (3). This property is associated, as in haloarchaea, with a high content of acidic amino acids and a low content of hydrophobic residues in bulk protein, necessary for protein solubility at such high ionic strength (4). Cell integrity requires high salt concentrations in both cases, and growth only occurs at Ͼ2 M NaCl. Both Salinibacter and the haloarchaea are aerobic heterotrophs that exploit the large stock of organic nutrients produced in previous stages of seawater concentration, mostly by the green alga Dunaliella, and they use a similar range of organic compounds as carbon and energy sources (5). Like haloarchaea, Salinibacter contains a high proportion of carotenoids in its membrane, pro...

Fine-scale evolution: genomic, phenotypic and ecological differentiation in two coexisting Salinibacter ruber strains

“…We will refer to these regions as the hypervariable regions HVR1 and HVR2 (as in Whilhelm et al (2007)). HVRs corresponded (see Figure 1, bottom and Supplementary Figure 2) with two of the three genomic islands previously described in S. ruber M31 (Mongodin et al, 2005) and could thus represent islands of high genomic variability in this species. A general terminology for hypervariable regions does not seem to exist, however, they are often referred to as 'islands' in analogy to pathogenicity islands, although genomic islands are usually considered to be mobile genetic elements (Dobrindt et al, 2004).…”

“…In good agreement, rapid annotations using subsystems technology analyses (Aziz et al, 2008) Comparative genomics of Salinibacter ruber strains A Peña et al of the subsystems 'potassium metabolism', 'membrane transport' and 'phosphorus metabolism' were highly enriched in the CR. These zone only contained genes present in both strains, including the transporters encoded in the 'halophilic island' that has previously been reported for S. ruber M31 (Mongodin et al, 2005). Codon usage indexes were rather constant along S. ruber genome, with the exception of HVRs in which genes with poorer indexes were concentrated.…”

“…The complete genome sequence of strain M8 was determined, analyzed and compared with the previously published M31 genome (Mongodin et al, 2005). The main results from these analyses are summarized in Table 1 and Figures 1 and 2.…”

“…LGT was found to be lower than initially anticipated (Mongodin et al, 2005). To increase the stringency of these analyses, we used a two-step approach to identify genes likely transferred to the M8 genome from Archaea (or the other way around).…”

“…For this purpose, the genome of strain M8 has been fully sequenced and compared with the previously sequenced M31 genome (type strain DSMZ 13855 T , Mongodin et al, 2005). Phenotypic differences between both strains were examined by metabolomic analysis using Fourier transform ion cyclotron resonance mass spectrometry .…”