Evolutionary timing of the origins of mesophilic sulphate reduction and oxygenic photosynthesis: a phylogenomic dating approach

Abstract

Until recently, the deep‐branching relationships in the bacterial domain have been unresolved. A new phylogenetic approach (termed compartmentalization) was able to resolve these deep‐branching relationships successfully by using a large number of genes from whole genome sequences and by reducing long branch attraction artefacts. This new, well‐resolved phylogenetic tree reveals the evolutionary relationships between diverse bacterial groups that leave important traces in the geological record. It shows that mesophilic sulphate reducers originated before the Cyanobacteria, followed by the origination of sulphur‐ and pyrite‐oxidizing bacteria after oxygen became available in the biosphere. This evolutionary pattern mirrors a similar pattern in the Palaeoproterozoic geological record. Sulphur isotopic fractionation records indicate that large‐scale bacterial sulphate reduction began in marine environments around 2.45 billion years ago (Ga), followed by rapid oxygenation of the atmosphere about 2.3 or 2.2 Ga. Oxygenation was then followed by increasing oceanic sulphate concentrations (probably owing to pyrite oxidation and continental weathering), which then resulted in the disappearance of banded iron formations by 1.8 Ga. The similarity between the phylogenetic and geological records suggests that the geochemical changes observed on the Palaeoproterozoic Earth were caused by major origination events in the mesophilic bacteria, and that these geochemical changes then caused additional origination events, such as aerobic respiration. If so, then constraints on divergence dates can be established for many microbial groups, including the Cyanobacteria, mesophilic bacteria, mesophilic sulphate reducers, methanotrophs, several anoxygenic phototrophs, as well as for mitochondrial endosymbiosis. These dates may also help to explain a large number of other changes in the geological record of the Neoarchean and Palaeoproterozoic Earth. This hypothesis, however, does not agree with the finding of cyanobacterial and eukaryote lipids at 2.7 Ga, and suggests that further work needs to be done to elucidate the discrepancies in both these areas.

A Post-Genomic View of the Ecophysiology, Catabolism and Biotechnological Relevance of Sulphate-Reducing Prokaryotes

“…For most of the Proterozoic, sulphate reduction was a dominant biological process in the oceans, where most evolutionary processes were taking place, and the deep ocean waters remained anoxic and sulphidic or ferruginous, overlaid by an oxygenated surface layer (Anbar & Knoll, 2002;Canfield, 1998;Canfield, Poulton, & Narbonne, 2007;Scott et al, 2008). Based on phylogenomic arguments, it has also been suggested that the mesophilic sulphate reducers evolved only after the rise in atmospheric oxygen levels (Blank, 2004(Blank, , 2009, which would also agree with the fact that this metabolic trait is not dispersed among prokaryotic organisms, and might have initially been restricted to some early branching thermophilic sulphate reducers. It seems also plausible that the precursor sulphur-metabolizing organisms were not sulphate reducers, but sulphite reducers or sulphur/sulphite disproportionators, as sulphur and sulphite may have been abundant in the early earth, originating from volcanic and hydrothermal SO 2 .…”

Geodynamic and metabolic cycles in the Hadean

“…But soil profiles lacking Fe III and the absence in rocks of the petrified polysaccharide-rich sheaths around fossil cells to be expected of cyanobacteria seem to point to a late or post Archaean age (Westall 2001(Westall , 2003(Westall , 2004. Indeed, Blank (2004) suggests that oxygenic photosynthesis did not emerge until immediately prior to the Great Oxidation Event at ca. 2.3 Ga (Holland, 2002).…”

Biogeochemical signatures through time as inferred from whole microbial genomes

“…Parsimony and distance analyses were performed on the combined matrices using PAUP version 4.0b (Swofford, 2002); compatibility and threshold parsimony analyses were applied using the Phylip software package (Felsenstein, 1993). We compared these results to published trees based on rRNA (Fox and others, 1980;Woese, 1987), concatenated protein datasets (Hansmann and Martin, 2000;Brown and others, 2001;Brochier and others, 2002;Matte-Tailiez and others, 2002), and other gene content methods (Gerstein, 1998;Gerstein and Hedgyi, 1998;Snel and others, 1999;Tekaia and others, 1999;Lin and Gerstein, 2000;Wolf and others, 2001;Bansal and Meyer, 2002;Clarke and others, 2002;Korbel and others, 2002;Li and others, 2002;Blank, 2004;Yang and others, 2005), and produced a consensus microbial tree of life based on this comparison. This tree does not represent a strict consensus, but simply our best estimate of phylogenetic relationships based on these disparate studies.…”

“…For the consensus tree, the two groups of gram positive bacteria (the firmicutes and the actinobacteria) were united based on their overall similar cell structure, in spite of the limited molecular support for this grouping (Brown and others, 2001;Wolf and others, 2001;Fu and Fu-Liu, 2002;Blank, 2004). Our resulting tree of life, shown in figure 2C, is broadly similar to that based on rRNA (for example: Fox and others, 1980;Woese, 1987) with the following exceptions: (1) the methanogenic archaea are united together based on whole genome analysis (Slesarev and House and others, 2003b;Yang and others, 2005); and (2) cyanobacteria have been placed as a sister group to the gram positive bacteria (Gerstein, 1998;Hansmann and Martin, 2000;Blank, 2004; this study). Our trees of composite organisms ( fig.…”