Globally distributed Myxococcota with photosynthesis gene clusters illuminate the origin and evolution of a potentially chimeric
Photosynthesis is a fundamental biogeochemical process, thought to be restricted to a few bacterial and eukaryotic phyla. However, understanding the origin and evolution of phototrophic organisms can be impeded and biased by the difficulties of cultivation. Here, we analyzed metagenomic datasets and found potential photosynthetic abilities encoded in the genomes of uncultivated bacteria within the phylum Myxococcota. A putative photosynthesis gene cluster encoding a type-II reaction center appears in at least six Myxococcota families from three classes, suggesting vertical inheritance of these genes from an early common ancestor, with multiple independent losses in other lineages. Analysis of metatranscriptomic datasets indicate that the putative myxococcotal photosynthesis genes are actively expressed in various natural environments. Furthermore, heterologous expression of myxococcotal pigment biosynthesis genes in a purple bacterium supports that the genes can drive photosynthetic processes. Given that predatory abilities are thought to be widespread across Myxococcota, our results suggest the intriguing possibility of a chimeric lifestyle (combining predatory and photosynthetic abilities) in members of this phylum.
a The cosmopolitan distribution of the photosynthesis gene-containing Myxococcota. Each genome is colored by its corresponding habitat and labeled with its taxonomic affiliation near corresponding geographical location. Fourteen MAGs (average completeness ~92.6%) possess (near) complete PGCs with 26~35 genes coding for all proteins of the RCs, enzymes of bacteriochlorophyll and carotenoid biosynthesis, regulatory proteins, and cofactors. Eight MAGs (average completeness ~85.3%) possess partial PGCs, consisting of either only one cluster with 12~24 photosynthesis genes or fragmented clusters dispersed in different contigs. Photosynthesis genes did not form apparent PGC (photosynthesis gene number <12 in any clusters) for the remaining 10 MAGs (average completeness ~84.6%), potentially attributed to incomplete assembly and/or binning of fragment reads in the next generation sequencing. b Sankey diagram shows the relationship between habitats and taxonomy of the photosynthesis gene-containing Myxococcota. c Gene organizations and phylogenies of representative myxococcotal PGCs. Genomic data was referenced for the PGC composition: the most closely related alphaproteobacterial genomes, Algihabitans albus HHTR 118 (GenBank accession no. GCA_003572205.1) and the genome belonging to the family Inquilinaceae (GEM accession no. 3300026561_2), the distantly related Gemmatimonadota genome Gemmatimonas sp. (GenBank accession no. GCA_020247115.1) and gammaproteobacterial genome Methyloversatilis discipulorum_A (GenBank accession no. GCA_018780585.1). Members from Alphaproteobacteria, Gammaproteobacteria, Gemmatimonadota, and Myxococcota are assigned different background colors. Photosynthesis genes are also colored: bch (green) and bci (purple), bacteriochlorophyll biosynthesis genes; puf (red), genes encoding reaction center proteins; puh (blue), genes encoding reaction center assembly proteins; crt (orange), carotenoid biosynthesis genes; gray, hypothetical genes or those of no relevance to phototrophy.
Colored parts in snowflake indicate the presence/absence of metabolic pathways and proteins for representative genome of each Myxococcota family. Half-filled parts in snowflake indicate the absence of proteins in the representative genome but present in other genomes from the same family. Gray color denotes the pathway or protein is absent in all genomes of this family. Representative genome of the family Nannocystaceae contains complete CBB cycle. Representative genomes of the families Myxococcaceae and Ca. Kuafubacteriaceae contain near complete CBB cycle with key enzymes, and sole missing enzymes can be identified in other genomes from corresponding family. The following metabolic pathways were used in the figure: bacteriochlorophyll synthesis pathway; TCA cycle, citrate cycle; glycolysis pathway; CBB cycle, Calvin-Benson-Bassham cycle; EMC, ethylmalonyl-CoA pathway; assimilatory sulfate reduction; dissimilatory nitrate reduction; carotenoid synthesis pathways, e.g., spheroidene pathway, astaxanthin biosynthesis pathway, and spirilloxanthin pathway. Several marker proteins were also included in the figure, e.g., proteorhodopsin; PufLM, photosynthetic reaction center subunits; form I RuBisCO, ribulose-1,5-bisphosphate carboxylase/oxygenase.
a Whole-cell absorption spectra of strains of Rba. sphaeroides. The wild-type (WT) spectrum has absorption features for LH2 and RC–LH1 that are missing in the ΔbciA ΔbchYZ mutant. Heterologous expression of bchYZ from LLY-WYZ−16_1 (Ca. Kuafubacteriaceae) in this mutant background restored the pigmentation of the WT (inset), and the assembly of LH2 and RC–LH1 as noted by the appearance of the absorption features of the photosynthetic complexes. b HPLC analysis of carotenoids extracted from Rba. sphaeroides strains. Heterologous expression of crtI from LLY-WYZ-10_1 (Nannocystaceae) in a mutant blocked at phytoene (ΔcrtIC) demonstrates that this gene functions as phytoene desaturase synthesizing both neurosporene and lycopene, as judged from their absorption spectra.