On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria

Soo, Rochelle M.; Hemp, James; Parks, Donovan H.; Fischer, Woodward W.; Hugenholtz, Philip

doi:10.1126/science.aal3794

Cited by 338 publications

(304 citation statements)

References 38 publications

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“…The absence of photosynthetic machinery in either of these outgroups is parsimonious with oxygenic photosynthesis evolving within the Cyanobacteria/Melainabacteria/Sericytochromatia (CMS) Group after the divergence of Melainabacteria, either via a fusion event via HGT of photosystems from other groups (Soo et al., ), or photosystem origin and duplication within this lineage itself (Allen & Martin, ). Due to the expansion of this lineage, the renaming of O 2 ‐producing Cyanobacteria to “Oxyphotobacteria” has been proposed to reflect the derived character of oxygenic photosynthesis acquired in the ancestor lineage of this group (Shih et al., ; Soo et al., ). By including the non‐photosynthetic lineages of the CMS Group, we are able to shorten the Cyanobacteria stem lineage along which RC HGT likely occurred and increase our ability to discriminate between specific HGT hypotheses.…”

Section: Introductionmentioning

confidence: 99%

Dating phototrophic microbial lineages with reticulate gene histories

et al. 2018

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Phototrophic bacteria are among the most biogeochemically significant organisms on Earth and are physiologically related through the use of reaction centers to collect photons for energy metabolism. However, the major phototrophic lineages are not closely related to one another in bacterial phylogeny, and the origins of their respective photosynthetic machinery remain obscured by time and low sequence similarity. To better understand the co‐evolution of Cyanobacteria and other ancient anoxygenic phototrophic lineages with respect to geologic time, we designed and implemented a variety of molecular clocks that use horizontal gene transfer (HGT) as additional, relative constraints. These HGT constraints improve the precision of phototroph divergence date estimates and indicate that stem green non‐sulfur bacteria are likely the oldest phototrophic lineage. Concurrently, crown Cyanobacteria age estimates ranged from 2.2 Ga to 2.7 Ga, with stem Cyanobacteria diverging ~2.8 Ga. These estimates provide a several hundred Ma window for oxygenic photosynthesis to evolve prior to the Great Oxidation Event (GOE) ~2.3 Ga. In all models, crown green sulfur bacteria diversify after the loss of the banded iron formations from the sedimentary record (~1.8 Ga) and may indicate the expansion of the lineage into a new ecological niche following the GOE. Our date estimates also provide a timeline to investigate the temporal feasibility of different photosystem HGT events between phototrophic lineages. Using this approach, we infer that stem Cyanobacteria are unlikely to be the recipient of an HGT of photosystem I proteins from green sulfur bacteria but could still have been either the HGT donor or the recipient of photosystem II proteins with green non‐sulfur bacteria, prior to the GOE. Together, these results indicate that HGT‐constrained molecular clocks are useful tools for the evaluation of various geological and evolutionary hypotheses, using the evolutionary histories of both genes and organismal lineages.

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Section: Introductionmentioning

confidence: 99%

Dating phototrophic microbial lineages with reticulate gene histories

et al. 2018

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“…Nonetheless, some cyanobacterial non-photosynthetic mutants have evolved as obligate endosymbionts . Although nonphotosynthetic bacteria such as Melainabacteria and Sericytochromatia have been included into the phylum 'cyanobacteria' (Soo et al, 2017), in our opinion they constitute different groups of organisms (see also Pakrasi and Zehr, 2017). Therefore, photoautotrophy is the characteristic mode of growth of cyanobacteria, although numerous strains in this phylum can use sugars supporting either chemoheterotrophic, mixotrophic or photoheterotrophic growth (Rippka et al, 1979;Nieves-Morión and Flores, 2018).…”

Section: Introductionmentioning

confidence: 99%

Genetic responses to carbon and nitrogen availability in Anabaena

Herrero

Flores

2018

Environmental Microbiology

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Heterocyst-forming cyanobacteria are filamentous organisms that perform oxygenic photosynthesis and CO fixation in vegetative cells and nitrogen fixation in heterocysts, which are formed under deprivation of combined nitrogen. These organisms can acclimate to use different sources of nitrogen and respond to different levels of CO . Following work mainly done with the best studied heterocyst-forming cyanobacterium, Anabaena, here we summarize the mechanisms of assimilation of ammonium, nitrate, urea and N , the latter involving heterocyst differentiation, and describe aspects of CO assimilation that involves a carbon concentration mechanism. These processes are subjected to regulation establishing a hierarchy in the assimilation of nitrogen sources -with preference for the most reduced nitrogen forms- and a dependence on sufficient carbon. This regulation largely takes place at the level of gene expression and is exerted by a variety of transcription factors, including global and pathway-specific transcriptional regulators. NtcA is a CRP-family protein that adjusts global gene expression in response to the C-to-N balance in the cells, and PacR is a LysR-family transcriptional regulator (LTTR) that extensively acclimates the cells to oxygenic phototrophy. A cyanobacterial-specific transcription factor, HetR, is involved in heterocyst differentiation, and other LTTR factors are specifically involved in nitrate and CO assimilation.

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“…In other words, lineages of phototrophs are often closely related to nonphotosynthetic lineages. Melainabacteria and Sericytochromatia lack genes that are involved in photosynthesis (Soo et al, 2017) and are likely to have lost the ability to perform photosynthesis after their divergence from Cyanobacteria. Melainabacteria and Sericytochromatia lack genes that are involved in photosynthesis (Soo et al, 2017) and are likely to have lost the ability to perform photosynthesis after their divergence from Cyanobacteria.…”

Section: The Origin Of Photosystem II (Psii) Vs the Origin Of Cymentioning

confidence: 99%

On the origin of oxygenic photosynthesis and Cyanobacteria

2019

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Summary Oxygenic phototrophs have played a fundamental role in Earth’s history by enabling the rise of atmospheric oxygen (O2) and paving the way for animal evolution. Understanding the origins of oxygenic photosynthesis and Cyanobacteria is key when piecing together the events around Earth’s oxygenation. It is likely that photosynthesis evolved within bacterial lineages that are not extant, so it can be challenging when studying the early history of photosynthesis. Recent genomic and molecular evolution studies have transformed our understanding about the evolution of photosynthetic reaction centres and the evolution of Cyanobacteria. The evidence reviewed here highlights some of the most recent advances on the origin of photosynthesis both at the genomic and gene family levels.

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On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria

Abstract: Oxygen-producing photosynthesis and oxygen-consuming respiration evolved after the divergence of the main lineages of blue-green algae.

Cited by 338 publications

References 38 publications

Dating phototrophic microbial lineages with reticulate gene histories

Dating phototrophic microbial lineages with reticulate gene histories

Genetic responses to carbon and nitrogen availability in Anabaena

On the origin of oxygenic photosynthesis and Cyanobacteria

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