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Granick Revisited: Synthesizing Evolutionary and Ecological Evidence for the Late Origin of Bacteriochlorophyll via Ghost Lineages and Horizontal Gene Transfer

View ORCID ProfileLewis M. Ward, Patrick M. Shih
doi: https://doi.org/10.1101/2020.09.01.277905
Lewis M. Ward
1Department of Earth and Planetary Sciences, Harvard University, Cambridge, MA, United States
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  • For correspondence: lewis_ward@fas.harvard.edu
Patrick M. Shih
2Department of Plant Biology, University of California, Davis, CA, USA
3Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
4Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA, USA
5Genome Center, University of California, Davis, Davis, CA, USA
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Abstract

Photosynthesis—both oxygenic and more ancient anoxygenic forms—has fueled the bulk of primary productivity on Earth since it first evolved more than 3.4 billion years ago. However, the early evolutionary history of photosynthesis has been challenging to interpret due to the sparse, scattered distribution of metabolic pathways associated with photosynthesis, long timescales of evolution, and poor sampling of the true environmental diversity of photosynthetic bacteria. Here, we reconsider longstanding hypotheses for the evolutionary history of phototrophy by leveraging recent advances in metagenomic sequencing and phylogenetics to analyze relationships among phototrophic organisms and components of their photosynthesis pathways, including reaction centers and individual proteins and complexes involved in the multi-step synthesis of (bacterio)-chlorophyll pigments. We demonstrate that components of the photosynthetic apparatus have undergone extensive, independent histories of horizontal gene transfer. This suggests an evolutionary mode by which modular components of phototrophy are exchanged between diverse taxa in a piecemeal process that has led to biochemical innovation. We hypothesize that the evolution of extant anoxygenic photosynthetic bacteria has been spurred by ecological competition and restricted niches following the evolution of oxygenic Cyanobacteria and the accumulation of O2 in the atmosphere, leading to the relatively late evolution of bacteriochlorophyll pigments and the radiation of diverse crown group anoxygenic phototrophs. This hypothesis expands on the classic “Granick hypothesis” for the stepwise evolution of biochemical pathways, synthesizing recent expansion in our understanding of the diversity of phototrophic organisms as well as their evolving ecological context through Earth history.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 03, 2020.
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Granick Revisited: Synthesizing Evolutionary and Ecological Evidence for the Late Origin of Bacteriochlorophyll via Ghost Lineages and Horizontal Gene Transfer
Lewis M. Ward, Patrick M. Shih
bioRxiv 2020.09.01.277905; doi: https://doi.org/10.1101/2020.09.01.277905
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Granick Revisited: Synthesizing Evolutionary and Ecological Evidence for the Late Origin of Bacteriochlorophyll via Ghost Lineages and Horizontal Gene Transfer
Lewis M. Ward, Patrick M. Shih
bioRxiv 2020.09.01.277905; doi: https://doi.org/10.1101/2020.09.01.277905

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