PHYLOGENETIC EVIDENCE FOR MASS EXTINCTIONS OF MICROBIAL ANOXYGENIC PHOTOTROPHS IN EARTH HISTORY

Anoxygenic phototrophy has a broad taxonomic distribution across microbial lineages, and very likely represents the ancestral physiological state of both oxygenic and oxygenic microbial phototroph systems. However, this distribution is relatively sparse, and phylogenetically consistent with major extant lineages, including green and purple bacteria, becoming more recently established via acquisition of phototrophic genes by horizontal gene transfer. The evolutionary history of the genes encoding photosynthetic machinery clearly reaches much more deeply, long before extant anoxygenic phototrophs diversified. Given current molecular clock estimates showing these clades emerging in the Paleoproterozoic, paleontological and geochemical evidence for phototrophy appears to be much older than expected. This evidence includes stromatolite reef formations as old as 3.5 Ga, various isotopic fractionations, and banded iron formations possibly formed by photoferrotrophs in Archean marine systems. This apparent paradox can be explained by there being an extinct diversity of anoxygenic phototrophs, wherein the groups responsible for Archean phototrophic paleobiosignatures left no descendants. Furthermore, the extant taxonomic distribution of microbial phototrophy and phototroph-specific physiological characters predicts several "missing" intermediate forms whose absence can only be explained by extinction. For example, a phototrophic sister group to Cyanobacteria preserving an anoxygenic ancestral state is conspicuously absent, as are basal, chlorosome-lacking green sulfur and nonsulfur bacteria, or any deeply-branching photoferrotrophic lineages. Taken together, this evidence is consistent with one or more major extinction events and/or biotic successions in dominant phototrophic groups during Earth's history. An accurate interpretation of the geological record of phototrophy and subsequent ecological reconstruction of Archean and Proterozoic planetary systems must take such extinctions into account.