Dataset Information

Mobile elements in a single-filament orange Guaymas Basin Beggiatoa ("Candidatus Maribeggiatoa") sp. draft genome: evidence for genetic exchange with cyanobacteria.

ABSTRACT: The draft genome sequence of a single orange Beggiatoa ("Candidatus Maribeggiatoa") filament collected from a microbial mat at a hydrothermal site in Guaymas Basin (Gulf of California, Mexico) shows evidence of extensive genetic exchange with cyanobacteria, in particular for sensory and signal transduction genes. A putative homing endonuclease gene and group I intron within the 23S rRNA gene; several group II catalytic introns; GyrB and DnaE inteins, also encoding homing endonucleases; multiple copies of sequences similar to the fdxN excision elements XisH and XisI (required for heterocyst differentiation in some cyanobacteria); and multiple sequences related to an open reading frame (ORF) (00024_0693) of unknown function all have close non-Beggiatoaceae matches with cyanobacterial sequences. Sequences similar to the uncharacterized ORF and Xis elements are found in other Beggiatoaceae genomes, a variety of cyanobacteria, and a few phylogenetically dispersed pleiomorphic or filamentous bacteria. We speculate that elements shared among filamentous bacterial species may have been exchanged in microbial mats and that some of them may be involved in cell differentiation.

SUBMITTER: MacGregor BJ

PROVIDER: S-EPMC3697557 | biostudies-literature | 2013 Jul

REPOSITORIES: biostudies-literature

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Mobile elements in a single-filament orange Guaymas Basin Beggiatoa ("Candidatus Maribeggiatoa") sp. draft genome: evidence for genetic exchange with cyanobacteria.

MacGregor Barbara J BJ Biddle Jennifer F JF Teske Andreas A

Applied and environmental microbiology 20130419 13

The draft genome sequence of a single orange Beggiatoa ("Candidatus Maribeggiatoa") filament collected from a microbial mat at a hydrothermal site in Guaymas Basin (Gulf of California, Mexico) shows evidence of extensive genetic exchange with cyanobacteria, in particular for sensory and signal transduction genes. A putative homing endonuclease gene and group I intron within the 23S rRNA gene; several group II catalytic introns; GyrB and DnaE inteins, also encoding homing endonucleases; multiple ...[more]

PMID: 23603674

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Project description:Orange filamentous Beggiatoaceae form massive microbial mats on hydrothermal sediments in Guaymas Basin; these bacteria are considered to oxidize sulfide with nitrate and nitrite as electron acceptors. From a previously analyzed genome of an orange Beggiatoaceae filament, three candidate genes for enzymes with nitrite-reducing function - an orange octaheme cytochrome, a nirS nitrite reductase, and a nitrite/tetrathionate-reducing octaheme cytochrome - were cloned and expressed in Escherichia coli. The expressed and purified orange cytochrome showed reduced nitrite-reducing activity compared to the multifunctional native protein obtained from microbial mats. The nirS gene product showed in vitro but no in-gel nitrite-reducing activity; and the nitrite/tetrathionate-reducing octaheme cytochrome was capable of reducing both nitrite and tetrathionate in vitro. Phylogenetic analysis shows that the orange Beggiatoaceae nirS, in contrast to the other candidate nitrite reductases, does not form monophyletic lineages with its counterparts in other large sulfur-oxidizing bacteria, and most likely represents a recent acquisition by lateral gene transfer. The nitrite/tetrathionate-reducing enzyme of the orange Beggiatoaceae is related to nitrite- and tetrathionate reductases harbored predominantly by Gammaproteobacteria, including obligate endosymbionts of hydrothermal vent tubeworms. Thus, the orange Guaymas Basin Beggiatoaceae have a repertoire of at least three different functional enzymes for nitrite reduction. By demonstrating the unusual diversity of enzymes with a potential role in nitrite reduction, we show that bacteria in highly dynamic, sulfide-rich hydrothermal vent habitats adapt to these conditions that usually prohibit nitrate and nitrite reduction. In the case of the orange Guaymas Beggiatoaceae, classical denitrification appears to be replaced by different multifunctional enzymes for nitrite and tetrathionate reduction; the resulting ecophysiological flexibility provides a new key to the dominance of these Beggiatoaceae in hydrothermal hot spots.

Project description:For multidomain proteins, evolutionary changes may occur at the domain as well as the whole-protein level. An example is presented here, with suggestions for how such complicated relationships might be visualized. Earlier analysis of the Candidatus Maribeggiatoa str. Orange Guaymas (BOGUAY; Gammaproteobacteria) single-filament draft genome found evidence of gene exchange with the phylogenetically distant Cyanobacteria, particularly for sensory and signal transduction proteins. Because these are modular proteins, known to undergo frequent duplication, domain swapping, and horizontal gene transfer, a single domain was chosen for analysis. Recognition (REC) domains are short (~125 amino acids) and well conserved, simplifying sequence alignments and phylogenetic calculations. Over 100 of these were identified in the BOGUAY genome and found to have a wide range of inferred phylogenetic relationships. Two sets were chosen here for detailed study. One set of four BOGUAY ORFs has closest relatives among other Beggiatoaceae and Cyanobacteria. A second set of four has REC domains with more mixed affiliations, including other Beggiatoaceae, several sulfate-reducing Deltaproteobacteria and Firmicutes, magnetotactic Nitrospirae, one Shewanella and one Ferrimonas strain (both Gammaproteobacteria), and numerous Vibrio vulnificus and V. navarrensis strains (also Gammaproteobacteria). For an overview of the possible origins of the whole proteins and the surrounding genomic regions, color-coded BLASTP results were produced and displayed against cartoons showing protein domain structure of predicted genes. This is suggested as a visualization method for investigation of possible horizontally transferred regions, giving more detail than scans of DNA composition and codon usage but much faster than carrying out full phylogenetic analyses for multiple proteins. As expected, most of the predicted sensor histidine kinases investigated have two or more segments with distinct BLASTP affiliations. For the first set of BOGUAY ORFs, the flanking regions were also examined, and the results suggest they are embedded in genomic stretches with complex histories. An automated method of creating such visualizations could be generally useful; a wish list for its features is given.

Dataset Information

Mobile elements in a single-filament orange Guaymas Basin Beggiatoa ("Candidatus Maribeggiatoa") sp. draft genome: evidence for genetic exchange with cyanobacteria.

Publications

Mobile elements in a single-filament orange Guaymas Basin Beggiatoa ("Candidatus Maribeggiatoa") sp. draft genome: evidence for genetic exchange with cyanobacteria.

Similar Datasets

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