Discovery of a free-living chlorophyll d -producing cyanobacterium with a hybrid proteobacterial/cyanobacterial small-subunit rRNA gene

Abstract

Chlorophyll d-producing cyanobacteria are a recently described group of phototrophic bacteria that is a major focus of photosynthesis research, previously known only from marine environments in symbiosis with eukaryotes. We have discovered a free-living member of this group from a eutrophic hypersaline lake. Phylogenetic analyses indicated these strains are closely related to each other but not to prochlorophyte cyanobacteria that also use an alternative form of chlorophyll as the major light-harvesting pigment. We have also demonstrated that these bacteria acquired a fragment of the small-subunit rRNA gene encoding a conserved hairpin in the bacterial ribosome from a proteobacterial donor at least 10 million years before the present. Thus, our most widely used phylogenetic marker can be a mosaic of sequence fragments with widely divergent evolutionary histories.cyanobacteria ͉ lateral gene transfer

Direct evidence for redundant segmental replacement between multiple 18S rRNA genes in a single Prototheca strain

“…Even if one of these scenarios did apply to strain ATCC 16529, it ought to be followed by further recombination of divergent gene fragments between intragenomic operons. Specifically, recombination is obviously necessary to form mosaic genes in the first scenario, but also in the second to explain the observed highly segmental nature of 18S rRNA genes, as loci for recombination via LGT between organisms are restricted in SSU rRNA genes (Wang & Zhang, 2000;Gogarten et al, 2002;Miller et al, 2005). In any case, it is plausible that a mobile genetic element-like mechanism (which works in a single genome) might play a role in the formation of the complex mosaic structure observed here.…”

“…Therefore, it is not clear whether or not LGT is responsible for the occurrence of identical base pairs in those hairpins of SSU rRNA in different actinomycetes. In the second case, two strains of a chlorophyll d-producing cyanobacterium have been found to have gained a single hairpin helix in variable region V1 of the SSU rRNA from a b-proteobacterium (Miller et al, 2005). In the third case, comparative sequence analysis of six rRNA operons of the actinomycete Thermomonospora chromagena has revealed that the SSU rRNA gene of one operon (rrnB) contains two or three regions that were likely derived from a different species, Thermobispora bispora, whereas sequences of the corresponding genes from the remaining five operons in T. chromagena (rrnA, rrnC, rrnD, rrnE and rrnF) are almost identical with each other and lack evidence for interspecific recombination (Yap et al, 1999;Gogarten et al, 2002).…”

“…interspecific LGT (Wang & Zhang, 2000;Gogarten et al, 2002;Miller et al, 2005). Even if one of these scenarios did apply to strain ATCC 16529, it ought to be followed by further recombination of divergent gene fragments between intragenomic operons.…”

“…Therefore, the potentially crucial biological function that the organism pursues via redundant segmental replacement of 18S rRNA genes has yet to be identified. Fixation and long-term maintenance of a single foreign gene fragment in an SSU rRNA gene was thought to have been favoured by natural selection (Miller et al, 2005), but this does not explain further recombination of 18S rRNA genes in a single genome. Sweeney et al (1996) inserted DNA fragments, which were complementary to the coding strands of protein-encoding genes, in the variable region of the large subunit (LSU) rRNA gene of the protist Tetrahymena thermophila.…”

“…Miller et al (2005) demonstrated that a chlorophyll d-producing cyanobacterium acquired a fragment of the SSU rRNA gene encoding a structurally conserved hairpin from a proteobacterial donor. This analysis was performed by computational statistical comparison of two likelihood models to account for the identical sequences in variable region 1 (V1) of the SSU rRNA genes of the cyanobacterium and certain proteobacteria: one for lateral gene transfer (LGT) and the other for convergent evolution.…”