Clustered Genes Related to Sulfate Respiration in Uncultured Prokaryotes Support the Theory of Their Concomitant Horizontal Transfer

Abstract

The dissimilatory reduction of sulfate is an ancient metabolic process central to today's biogeochemical cycling of sulfur and carbon in marine sediments. Until now its polyphyletic distribution was most parsimoniously explained by multiple horizontal transfers of single genes rather than by a not-yet-identified "metabolic island." Here we provide evidence that the horizontal transfer of a gene cluster may indeed be responsible for the patchy distribution of sulfate-reducing prokaryotes (SRP) in the phylogenetic tree. We isolated three DNA fragments (32 to 41 kb) from uncultured, closely related SRP from DNA directly extracted from two distinct marine sediments. Fosmid ws39f7, and partially also fosmids ws7f8 and hr42c9, harbored a core set of essential genes for the dissimilatory reduction of sulfate, including enzymes for the reduction of sulfur intermediates and synthesis of the prosthetic group of the dissimilatory sulfite reductase. Genome comparisons suggest that encoded membrane proteins universally present among SRP are critical for electron transfer to cytoplasmic enzymes. In addition, novel, conserved hypothetical proteins that are likely involved in dissimilatory sulfate reduction were identified. Based on comparative genomics and previously published experimental evidence, a more comprehensive model of dissimilatory sulfate reduction is presented. The observed clustering of genes involved in dissimilatory sulfate reduction has not been previously found. These findings strongly support the hypothesis that genes responsible for dissimilatory sulfate reduction were concomitantly transferred in a single event among prokaryotes. The acquisition of an optimized gene set would enormously facilitate a successful implementation of a novel pathway.

Phylogeny of the alpha and beta subunits of the dissimilatory adenosine-5′-phosphosulfate (APS) reductase from sulfate-reducing prokaryotes – origin and evolution of the dissimilatory sulfate-reduction pathway

“…However, Syntrophobacter fumaroxidans harbours a second and functionally complete qmoABC operon that is not associated with the sat-aprBAqmoAB gene cluster. A separately transcribed qmoC homologue is present near the qmoAB and sat-aprBA gene loci in the metagenomic sequences of the LGT-affected unclassified putative SRB strains (fosws39f7, fosws7f8) (Mussmann et al, 2005). Interestingly, these strains are also closely related in the QmoA-and QmoB-based phylogenetic trees (not shown).…”

“…The evolution of the sulfate-respiration process in SRP has primarily been investigated by comparative phylogenetic studies of the dissimilatory sulfite reductase DsrAB, and this has confirmed the occurrence of multiple events of LGT of dsrAB among members of this physiological group (Klein et al, 2001;Mussmann et al, 2005;Zverlov et al, 2005). A widespread dispersal via 'metabolic islands' has recently been discussed as responsible for the polyphyletic distribution of this metabolic trait (Klein et al, 2001;Mussmann et al, 2005). In contrast to the comprehensive analysis of DsrAB phylogeny, knowledge concerning the evolution of the dissimilatory APS reductase is currently restricted to a single phylogenetic study based on the limited sequence information of a minor part of the aprA gene-coding region (~0?9 kb) from 60 taxonomically different SRP species (Friedrich, 2002).…”

“…The evolution of the sulfate-respiration process in SRP has primarily been investigated by comparative phylogenetic studies of the dissimilatory sulfite reductase DsrAB, and this has confirmed the occurrence of multiple events of LGT of dsrAB among members of this physiological group (Klein et al, 2001;Mussmann et al, 2005;Zverlov et al, 2005). A widespread dispersal via 'metabolic islands' has recently been discussed as responsible for the polyphyletic distribution of this metabolic trait (Klein et al, 2001;Mussmann et al, 2005).…”

“…A donor lineage for the LGT of their apr genes is not apparent. Interestingly, a congruent taxonomical classification of both uncultivated putative SRB strains (fosws39f7, fosws7f8) (Mussmann et al, 2005) was not possible on the basis of the Dsr and Apr sequences. A distinct origin is proposed for their xenologous apr and dsr genes, which are arranged as a metabolic island.…”

Biogeography and phylogenetic diversity of a cluster of exclusively marine myxobacteria

“…Fosmid library construction and screening for MMC 16S rRNA genes A fosmid library with DNA from surface sediment of an intertidal sand flat of the German Wadden Sea (see above) was constructed as described by Mussmann et al (2005) using the EpiFOS fosmid library production kit (Epicenter, Madison, WI, USA) according to the manufacturer's instructions. In total, 11 000 clones from the fosmid library were screened for MMC 16S rRNA genes using the primer pair MMC655f/MMC841r (see above).…”