The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages

Fournier, Gregory P.; Moore, Kelsey; Rangel, Luiz Thibério; Payette, Jack; Momper, Lily; Bosak, Tanja

doi:10.1098/rspb.2021.0675

Cited by 58 publications

(63 citation statements)

References 69 publications

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“…More calibrations, particularly maximum age constraints and calibrations within Archaea, are essential to refine the current estimates. Given the difficulties in establishing maximum ages for archaeal and bacterial clades, constraints from other sources such as donor-recipient age constraints inferred from HGTs ( Davín et al, 2018 ; Fournier et al, 2021 ; Szöllősi et al, 2021 ; Wolfe and Fournier, 2018 ), or clock models that capture biological opinion about rate shifts in early evolution, may be particularly valuable.…”

Section: Resultsmentioning

confidence: 99%

An estimate of the deepest branches of the tree of life from ancient vertically evolving genes

Moody

Mahendrarajah

Dombrowski

et al. 2022

eLife

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Core gene phylogenies provide a window into early evolution, but different gene sets and analytical methods have yielded substantially different views of the tree of life. Trees inferred from a small set of universal core genes have typically supported a long branch separating the archaeal and bacterial domains. By contrast, recent analyses of a broader set of non-ribosomal genes have suggested that Archaea may be less divergent from Bacteria, and that estimates of inter-domain distance are inflated due to accelerated evolution of ribosomal proteins along the inter-domain branch. Resolving this debate is key to determining the diversity of the archaeal and bacterial domains, the shape of the tree of life, and our understanding of the early course of cellular evolution. Here, we investigate the evolutionary history of the marker genes key to the debate. We show that estimates of a reduced Archaea-Bacteria (AB) branch length result from inter-domain gene transfers and hidden paralogy in the expanded marker gene set. By contrast, analysis of a broad range of manually curated marker gene datasets from an evenly sampled set of 700 Archaea and Bacteria reveal that current methods likely underestimate the AB branch length due to substitutional saturation and poor model fit; that the best-performing phylogenetic markers tend to support longer inter-domain branch lengths; and that the AB branch lengths of ribosomal and non-ribosomal marker genes are statistically indistinguishable. Furthermore, our phylogeny inferred from the 27 highest-ranked marker genes recovers a clade of DPANN at the base of the Archaea, and places CPR within Bacteria as the sister group to the Chloroflexota.

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Section: Resultsmentioning

confidence: 99%

An estimate of the deepest branches of the tree of life from ancient vertically evolving genes

Moody

Mahendrarajah

Dombrowski

et al. 2022

eLife

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“…Nevertheless, the clear history of rTCA cycle proteins within Chlorobiales, and the fidelity of their inheritance in several subgroups, permits the potential dating of carbon fixation within this clade. Recent molecular clock studies have produced age estimates for major divergences within Chlorobiales informed by large protein sequence datasets, cyanobacterial fossil calibrations, and HGT constraints 13 . These ages show crown Chlorobiales diversifying between 1977 Ma and 1607 Ma, and subsequent diversification of non- Chloroherpeton autotrophic lineages between 1300 Ma and 988 Ma (Figure 11).…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, new geochemical arguments have suggested a cyanobacterial origin for the fossil biomarkers found in Proterozoic depositional settings 11 . This brings the presence of GSB at 1.64 Ga into question, as well as the practice of using these biomarkers as a calibration for dating Chlorobiales in molecular clock analyses 12,13 .…”

Section: Introductionmentioning

confidence: 99%

“…There are six known modern biological pathways used by organisms to fix CO 2 . Most fractionate carbon differently, variably offsetting carbon isotope (δ 13 C) values of inorganic and organic carbon in the isotopic record 14,15 . Through this bulk signaling of δ 13 C sources, a cycle’s input can be mathematically inferred by isotopic mass balance of its components 16 .…”

Section: Introductionmentioning

confidence: 99%

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Chimeric Inheritance and Crown-Group Acquisitions of Carbon Fixation Genes within Chlorobiales

Paoletti

Fournier

2022

Preprint

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The geological record of microbial metabolisms and ecologies primarily consists of stable isotope fractionations and the diagenetic products of biogenic lipids. Carotenoid lipid biomarkers are particularly useful proxies for reconstructing this record, providing information on microbial phototroph primary productivity, redox couples, and oxygenation. The biomarkers okenane, chlorobactane, and isorenieratene are generally considered to be evidence of anoxygenic phototrophs, and provide a record that extends to ~1.64 Ga. The utility of the carotenoid biomarker record may be enhanced by examining the carbon isotopic ratios in these products, which are diagnostic for specific pathways of biological carbon fixation found today within different microbial groups. However, this joint inference assumes that microbes have conserved these pathways across the duration of the preserved biomarker record. Testing this hypothesis, we performed phylogenetic analyses of the enzymes constituting the reductive tricarboxylic acid (rTCA) cycle in Chlorobiales, the group of anoxygenic phototrophic bacteria usually implicated in the deposition of chlorobactane and isorenieretane. We find phylogenetically incongruent patterns of inheritance across all enzymes, indicative of horizontal gene transfers to both stem and crown Chlorobiales from multiple potential donor lineages. This indicates that a complete rTCA cycle was independently acquired at least twice within Chlorobiales and was not present in the last common ancestor. When combined with recent molecular clock analyses, these results predict that the Mesoproterzoic lipid biomarker record diagnostic for Chlorobiales should not preserve isotopic fractionations indicative of a full rTCA cycle. Furthermore, we conclude that coupling isotopic and biomarker records is insufficient for reliably reconstructing microbial paleoecologies in the absence of a complementary and consistent phylogenomic narrative.

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“…Cyanobacteria are the oldest known lineage of oxygen-releasing photosynthetic organisms ( Fournier et al, 2021 ). Oxygenic photosynthesis, which was first invented by cyanobacteria, is widely thought to have led to the ancient conversion of the reducing atmosphere into an oxidizing one ( Nealson and Myers, 1990 ; Wang et al, 2017 ; Catling and Zahnle, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Regulation and Functional Complexity of the Chlorophyll-Binding Protein IsiA

et al. 2021

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As the oldest known lineage of oxygen-releasing photosynthetic organisms, cyanobacteria play the key roles in helping shaping the ecology of Earth. Iron is an ideal transition metal for redox reactions in biological systems. Cyanobacteria frequently encounter iron deficiency due to the environmental oxidation of ferrous ions to ferric ions, which are highly insoluble at physiological pH. A series of responses, including architectural changes to the photosynthetic membranes, allow cyanobacteria to withstand this condition and maintain photosynthesis. Iron-stress-induced protein A (IsiA) is homologous to the cyanobacterial chlorophyll (Chl)-binding protein, photosystem II core antenna protein CP43. IsiA is the major Chl-containing protein in iron-starved cyanobacteria, binding up to 50% of the Chl in these cells, and this Chl can be released from IsiA for the reconstruction of photosystems during the recovery from iron limitation. The pigment–protein complex (CPVI-4) encoded by isiA was identified and found to be expressed under iron-deficient conditions nearly 30years ago. However, its precise function is unknown, partially due to its complex regulation; isiA expression is induced by various types of stresses and abnormal physiological states besides iron deficiency. Furthermore, IsiA forms a range of complexes that perform different functions. In this article, we describe progress in understanding the regulation and functions of IsiA based on laboratory research using model cyanobacteria.

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The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages

Cited by 58 publications

References 69 publications

An estimate of the deepest branches of the tree of life from ancient vertically evolving genes

An estimate of the deepest branches of the tree of life from ancient vertically evolving genes

Chimeric Inheritance and Crown-Group Acquisitions of Carbon Fixation Genes within Chlorobiales

Regulation and Functional Complexity of the Chlorophyll-Binding Protein IsiA

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