Phylogeny of Anoxygenic Photosynthesis Based on Sequences of Photosynthetic Reaction Center Proteins and a Key Enzyme in Bacteriochlorophyll Biosynthesis, the Chlorophyllide Reductase

Abstract

Photosynthesis is a key process for the establishment and maintenance of life on earth, and it is manifested in several major lineages of the prokaryote tree of life. The evolution of photosynthesis in anoxygenic photosynthetic bacteria is of major interest as these have the most ancient roots of photosynthetic systems. The phylogenetic relations between anoxygenic phototrophic bacteria were compared on the basis of sequences of key proteins of the type-II photosynthetic reaction center, including PufLM and PufH (PuhA), and a key enzyme of bacteriochlorophyll biosynthesis, the light-independent chlorophyllide reductase BchXYZ. The latter was common to all anoxygenic phototrophic bacteria, including those with a type-I and those with a type-II photosynthetic reaction center. The phylogenetic considerations included cultured phototrophic bacteria from several phyla, including Proteobacteria (138 species), Chloroflexi (five species), Chlorobi (six species), as well as Heliobacterium modesticaldum (Firmicutes), Chloracidobacterium acidophilum (Acidobacteria), and Gemmatimonas phototrophica (Gemmatimonadetes). Whenever available, type strains were studied. Phylogenetic relationships based on a photosynthesis tree (PS tree, including sequences of PufHLM-BchXYZ) were compared with those of 16S rRNA gene sequences (RNS tree). Despite some significant differences, large parts were congruent between the 16S rRNA phylogeny and photosynthesis proteins. The phylogenetic relations demonstrated that bacteriochlorophyll biosynthesis had evolved in ancestors of phototrophic green bacteria much earlier as compared to phototrophic purple bacteria and that multiple events independently formed different lineages of aerobic phototrophic purple bacteria, many of which have very ancient roots. The Rhodobacterales clearly represented the youngest group, which was separated from other Proteobacteria by a large evolutionary gap.

Distribution of Phototrophic Purple Nonsulfur Bacteria in Massive Blooms in Coastal and Wastewater Ditch Environments

“…Smaller numbers of the phylotypes were classified as members of Betaproteobacteria, Gemmatimonadetes, and unidentified phylogenetic groups. Phylotypes 12 and 16, assigned to Gemmatimonadetes and Betaproteobacteria, respectively, nested into the clade of Alphaproteobacteria, which can be explained by ancestral lateral transfer of a photosynthetic gene set with pufM from phototrophic alphaproteobacteria [57,59,60]. Except for the Gemmatimonadetes (phylotype 12), Dinoroseobacter (phylotype 15), and unidentified clones, all of the pufM clones detected could be assigned to members of PSB and PNSB.…”

Biogeochemical and omic evidence for paradoxical methane production via multiple co-occurring mechanisms in aquatic ecosystems

“…Notably, both DPOR and COR are nitrogenase-like enzymes (Nomata et al 2006, Chew & Bryant 2007, Tsukatani et al 2013, and both were abundant in all metatranscriptomes and metagenomes. DPOR and COR were particularly common within the Limnohabitans and Polynucleobacter genera, as some strains of these abundant freshwater bacteria are capable of performing aerobic anoxygenic photosynthesis (Kasalický et al 2018, Imhoff et al 2019, Hahn et al 2017. DPOR exclusively was also found in several cyanobacterial groups-such as Pseudanabaena, Dolichospermum, Gloeomargarita and Oscillatoria-in the metatranscriptome data.…”

“…We found that phnJ genes commonly clustered with other phn genes on the same contigs, particularly those from the Comamonadaceae. For example, contigs >50 kb containing phnC, phnD, phnE, phnI, phnJ, phnK, phnL, phnM were present in metagenomes from the LG2 and L6 incubations, and were affiliated with the abundant freshwater bacterial group Limnohabitans (Newton et al 2011, Kasalický et al 2018, Imhoff et al 2019, as well as other members of the Comamonadaceae, such as Hydrogenophaga and Acidovorax. Several longer contigs also contained pst or pho genes involved in P uptake and metabolism.…”

“…We propose that, similar to the findings of Zheng et al (2018), the nitrogenase-like enzymes DPOR and COR may be able to catalyze the reduction of CO2 into CH4. Importantly, these enzymes are present in Cyanobacteria as well as the abundant and ubiquitous freshwater bacterial groups Limnohabitans and Polynucleobacter (Kasalický et al 2018, Imhoff et al 2019, Hahn et al 2017).…”

“…We found that this mechanism was not limited to the Cyanobacteria, as the majority of DPOR and COR transcripts and genes were derived from several members of the Proteobacteria. This has multiple implications, as Limnohabitans and Polynucleobacter are among the most abundant and ubiquitous bacteria found in freshwater ecosystems (Newton et al 2011, Kasalický et al 2018, Imhoff et al 2019, Hahn et al 2017. Although there is significant genomic diversity within these groups (Newton et al 2011, Kasalický et al 2013, Hahn et al 2016, this suggests that the potential for CH4 production via this pathway may be widespread in freshwater.…”