3:50 PM - 4:10 PM
[BBG01-07] Discovery of a Chloroflexota phototroph with a Type I reaction center sheds new light on the evolution of photosynthesis
★Invited Papers
Keywords:Photosynthesis, Evolution, Biogeochemistry, Limnology, Metagenomics, Microbiology
The early Earth oceans of the Archaean Eon (approximately 3.8-2.5 billion years ago) are thought to have been anoxic, rich in dissolved iron(II), and poor in sulfide. Photosynthetic microorganisms likely proliferated in these environments and provided fixed carbon for early ecosystems. Unlike the modern Earth, where oxygenic phototrophs dominate surface ecosystems, anoxygenic phototrophic bacteria are thought to have been the main form of phototrophic life for much of the Archaean. In particular, iron(II)-oxidizing anoxygenic phototrophs, called photoferrotrophs, have been implicated in the deposition of Archaean Banded Iron Formations. However, on the modern Earth, permanently anoxic and ferruginous (i.e., iron(II)-rich and sulfide-poor) aquatic habitats are rare, and only a few such environments have been studied. The modern role of photoferrotrophy, along with the ancestral phototrophic life that might inhabit ferruginous ecosystems, remain poorly understood and limit understanding of early life on Earth.
To probe the diversity of phototrophic life in ferruginous environments, we sampled Lake 227, a seasonally anoxic and ferruginous Boreal Shield lake at the IISD-Experimental Lakes Area (Canada). By gradually amending anoxic lake water with iron(II)-containing freshwater medium, we enriched a highly novel anoxygenic phototroph, provisionally named, "Candidatus Chlorohelix allophototropha", that represents a novel order in the Chloroflexota (formerly Chloroflexi) phylum. This unique organism uses a Type I photosynthetic reaction center (RCI) despite placing phylogenetically sister to anoxygenic phototrophs using a Type II photosynthetic reaction center (RCII), revising our understanding of the evolution and ecology of photosynthesis.
"Ca. Chx. allophototropha" shows light-dependent growth and contains bacteriochlorophylls c and a, like known RCII-utilizing Chloroflexota members, based on HPLC and epifluorescence microscopy data. The complete genome of the strain lacks RCII-related genes and instead encodes a highly novel homolog of the pscA-like RCI gene. This novel pscA-like gene represents a distinct fifth clade of RCI, based on phylogenetic analysis, and places near the presumed root of the RCI phylogeny. Prior to the discovery of "Ca. Chx. allophototropha", each bacterial phylum containing anoxygenic phototrophs was associated with only a single class of photosynthetic reaction center. We now know that phylogenetically adjacent orders in the Chloroflexota contain phototrophs using RCI or RCII. Consistently sister phylogenetic placement of photosynthesis accessory genes of "Ca. Chx. allophototropha" and RCII-utilizing Chloroflexota members demonstrates that these two groups have shared phototrophic ancestry despite their unique phototrophic modes. Such a finding is directly relevant to understanding the origin of oxygenic photosynthesis, the only known phototrophic process to use RCII and RCI in tandem (as Photosystems II and I).
We detected RCI-containing relatives of "Ca. Chx. allophototropha" in four of eight Boreal Shield lakes that we surveyed using metagenome sequencing. Metatranscriptome data from two of the lakes demonstrate that "Ca. Chx. allophototropha" relatives can be among the top 10 most active microbial populations in Boreal Shield lake anoxic water columns while actively expressing photosynthesis genes. Growth of the "Ca. Chx. allophototropha" enrichment culture in iron(II)-containing autotrophic medium, together with accumulation of iron(III) in mature cultures, suggests that the culture is capable of photoferrotrophy. Together, these findings demonstrate that, although overlooked previously, "Ca. Chx. allophototropha" is highly relevant to the biogeochemistry of iron-rich ecosystems. Study of "Ca. Chx. allophototropha" will shed light on the potential function of Earth's early microbial communities and the evolutionary processes that led to the modern distribution of phototrophic life on Earth.
To probe the diversity of phototrophic life in ferruginous environments, we sampled Lake 227, a seasonally anoxic and ferruginous Boreal Shield lake at the IISD-Experimental Lakes Area (Canada). By gradually amending anoxic lake water with iron(II)-containing freshwater medium, we enriched a highly novel anoxygenic phototroph, provisionally named, "Candidatus Chlorohelix allophototropha", that represents a novel order in the Chloroflexota (formerly Chloroflexi) phylum. This unique organism uses a Type I photosynthetic reaction center (RCI) despite placing phylogenetically sister to anoxygenic phototrophs using a Type II photosynthetic reaction center (RCII), revising our understanding of the evolution and ecology of photosynthesis.
"Ca. Chx. allophototropha" shows light-dependent growth and contains bacteriochlorophylls c and a, like known RCII-utilizing Chloroflexota members, based on HPLC and epifluorescence microscopy data. The complete genome of the strain lacks RCII-related genes and instead encodes a highly novel homolog of the pscA-like RCI gene. This novel pscA-like gene represents a distinct fifth clade of RCI, based on phylogenetic analysis, and places near the presumed root of the RCI phylogeny. Prior to the discovery of "Ca. Chx. allophototropha", each bacterial phylum containing anoxygenic phototrophs was associated with only a single class of photosynthetic reaction center. We now know that phylogenetically adjacent orders in the Chloroflexota contain phototrophs using RCI or RCII. Consistently sister phylogenetic placement of photosynthesis accessory genes of "Ca. Chx. allophototropha" and RCII-utilizing Chloroflexota members demonstrates that these two groups have shared phototrophic ancestry despite their unique phototrophic modes. Such a finding is directly relevant to understanding the origin of oxygenic photosynthesis, the only known phototrophic process to use RCII and RCI in tandem (as Photosystems II and I).
We detected RCI-containing relatives of "Ca. Chx. allophototropha" in four of eight Boreal Shield lakes that we surveyed using metagenome sequencing. Metatranscriptome data from two of the lakes demonstrate that "Ca. Chx. allophototropha" relatives can be among the top 10 most active microbial populations in Boreal Shield lake anoxic water columns while actively expressing photosynthesis genes. Growth of the "Ca. Chx. allophototropha" enrichment culture in iron(II)-containing autotrophic medium, together with accumulation of iron(III) in mature cultures, suggests that the culture is capable of photoferrotrophy. Together, these findings demonstrate that, although overlooked previously, "Ca. Chx. allophototropha" is highly relevant to the biogeochemistry of iron-rich ecosystems. Study of "Ca. Chx. allophototropha" will shed light on the potential function of Earth's early microbial communities and the evolutionary processes that led to the modern distribution of phototrophic life on Earth.