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Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5'-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes

Jan Kuever

Max-Planck-Institute for Marine Microbiology, Celsiusstrasse 1, D-28359 Bremen, Germany

Correspondence
Jan Kuever
kuever{at}mpa-bremen.de

Dissimilatory adenosine-5'-phosphosulfate (APS) reductase (AprBA) is a key enzyme of the dissimilatory sulfate-reduction pathway. Homologues have been found in photo- and chemotrophic sulfur-oxidizing prokaryotes (SOP), in which they are postulated to operate in the reverse direction, oxidizing sulfite to APS. Newly developed PCR assays allowed the amplification of 92–93 % (2.1–2.3 kb) of the APS reductase locus aprBA. PCR-based screening of 116 taxonomically divergent SOP reference strains revealed a distribution of aprBA restricted to photo- and chemotrophs with strict anaerobic or at least facultative anaerobic lifestyles, including Chlorobiaceae, Chromatiaceae, Thiobacillus, Thiothrix and invertebrate symbionts. In the AprBA-based tree, the SOP diverge into two distantly related phylogenetic lineages, Apr lineages I and II, with the proteins of lineage II (Chlorobiaceae and others) in closer affiliation to the enzymes of the sulfate-reducing prokaryotes (SRP). This clustering is discordant with the dissimilatory sulfite reductase (DsrAB) phylogeny and indicates putative lateral aprBA gene transfer from SRP to the respective SOB lineages. In support of lateral gene transfer (LGT), several beta- and gammaproteobacterial species harbour both aprBA homologues, the DsrAB-congruent ‘authentic’ and the SRP-related, LGT-derived gene loci, while some relatives possess exclusively the SRP-related apr genes as a possible result of resident gene displacement by the xenologue. The two-gene state might be an intermediate in the replacement of the resident essential gene. Collected genome data demonstrate the correlation between the AprBA tree topology and the composition/arrangement of the apr gene loci (occurrence of qmoABC or aprM genes) from SRP and SOP of lineages I and II. The putative functional role of the SRP-related APS reductases in photo- and chemotrophic SOP is discussed.

Present Address: Bremen Institute for Materials Testing, Paul-Feller-Strasse 1, D-28199 Bremen, Germany.

The GenBank/EMBL/DDBJ accession numbers for the aprBA and 16S rRNA sequences of the species examined in this study are EF641902–EF641963 and EF675611–EF675615, respectively.

A supplementary table of the presence of genes encoding dissimilatory sulfite reductase and its functionally associated proteins in genome sequences of SOB, and two supplementary figures showing a phylogenetic consensus tree based on 16S rRNA gene sequences from the apr-containing SOB reference strains, and an AprB and AprA alignment showing indels among selected representatives of the major phylogenetic SOB lineages, are available with the online version of this paper.

This article has been cited by other articles:

				B. Meyer and J. Kuever Molecular Analysis of the Diversity of Sulfate-Reducing and Sulfur-Oxidizing Prokaryotes in the Environment, Using aprA as Functional Marker Gene Appl. Envir. Microbiol., December 1, 2007; 73(23): 7664 - 7679. [Abstract] [Full Text] [PDF]