Title: Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

Abstract

We report various lines of evidence from both comparative biology and the geologic record make it clear that the biochemical machinery for anoxygenic photosynthesis was present on early Earth and provided the evolutionary stock from which oxygenic photosynthesis evolved ca. 2.3 billion years ago. However, the taxonomic identity of these early anoxygenic phototrophs is uncertain, including whether or not they remain extant. Several phototrophic bacterial clades are thought to have evolved before oxygenic photosynthesis emerged, including the Chloroflexi, a phylum common across a wide range of modern environments. Although Chloroflexi have traditionally been thought to be an ancient phototrophic lineage, genomics has revealed a much greater metabolic diversity than previously appreciated. Here, using a combination of comparative genomics and molecular clock analyses, we show that phototrophic members of the Chloroflexi phylum are not particularly ancient, having evolved well after the rise of oxygen (ca. 867 million years ago), and thus cannot be progenitors of oxygenic photosynthesis. Similarly, results show that the carbon fixation pathway that defines this clade—the 3-hydroxypropionate bicycle—evolved late in Earth history as a result of a series of horizontal gene transfer events, explaining the lack of geological evidence for this pathway based on the carbon isotope record.more » Finally, these results demonstrate the role of horizontal gene transfer in the recent metabolic innovations expressed within this phylum, including its importance in the development of a novel carbon fixation pathway.« less

Authors:

Shih, Patrick M. ^[1]; Ward, Lewis M.  ^[2];

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Fischer, Woodward W. ^[2]

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+ Show Author Affiliations

1. Feedstocks Division, Joint BioEnergy Institute, Emeryville, CA 94608,, Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720,
2. Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, CA 91125

Publication Date:

2017-09-18

Research Org.:

Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Org.:

USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:

1392687

Alternate Identifier(s):

OSTI ID: 1426736

Grant/Contract Number:  

AC02-05CH11231

Resource Type:

Published Article

Journal Name:

Proceedings of the National Academy of Sciences of the United States of America

Additional Journal Information:

Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 114 Journal Issue: 40; Journal ID: ISSN 0027-8424

Publisher:

Proceedings of the National Academy of Sciences

Country of Publication:

United States

Language:

English

Subject:

59 BASIC BIOLOGICAL SCIENCES; 58 GEOSCIENCES; carbon fixation; phototrophy; molecular clock; comparative genomics