Metabolic connectivity as a driver of host and endosymbiont integration
Edited by Patrick J. Keeling, University of British Columbia, Vancouver, Canada, and accepted by the Editorial Board March 6, 2015 (received for review December 19, 2014)
Abstract
The origin of oxygenic photosynthesis in the Archaeplastida common ancestor was foundational for the evolution of multicellular life. It is very likely that the primary endosymbiosis that explains plastid origin relied initially on the establishment of a metabolic connection between the host cell and captured cyanobacterium. We posit that these connections were derived primarily from existing host-derived components. To test this idea, we used phylogenomic and network analysis to infer the phylogenetic origin and evolutionary history of 37 validated plastid innermost membrane (permeome) metabolite transporters from the model plant Arabidopsis thaliana. Our results show that 57% of these transporter genes are of eukaryotic origin and that the captured cyanobacterium made a relatively minor (albeit important) contribution to the process. We also tested the hypothesis that the bacterium-derived hexose-phosphate transporter UhpC might have been the primordial sugar transporter in the Archaeplastida ancestor. Bioinformatic and protein localization studies demonstrate that this protein in the extremophilic red algae Galdieria sulphuraria and Cyanidioschyzon merolae are plastid targeted. Given this protein is also localized in plastids in the glaucophyte alga Cyanophora paradoxa, we suggest it played a crucial role in early plastid endosymbiosis by connecting the endosymbiont and host carbon storage networks. In summary, our work significantly advances understanding of plastid integration and favors a host-centric view of endosymbiosis. Under this view, nuclear genes of either eukaryotic or bacterial (noncyanobacterial) origin provided key elements of the toolkit needed for establishing metabolic connections in the primordial Archaeplastida lineage.
Acknowledgments
This research was funded by National Science Foundation Grants 0936884 and 1317114 (to D.B.). A.P.M.W. appreciates support from the Deutsche Forschungsgemeinschaft (Grants EXC 1028 and WE 2231/8-2).
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Cover image: Pictured are two examples of endosymbiosis. In the center and at the four corners are Durinskia, a symbiotic consortium of a dinoflagellate and a diatom resulting in a complex cell, including multiple organelles from both partners. At the four cardinal points are images depicting an endosymbiosis between cicada cells and the bacterial endosymbionts Sulcia (outer ring) and Hodgkinia (inner circle), which together supply the insect with essential amino acids. The Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of Organelles Sackler Colloquium explores the processes by which endosymbiosis leads to repeated genetic and cellular integration across the tree of life. See the Introduction to the Sackler Colloquium by Patrick J. Keeling, John P. McCutcheon, and W. Ford Doolittle on pages 10101–10103. Images of Durinskia courtesy of Patrick J. Keeling; images of cicada cells courtesy of James Van Leuven and John P. McCutcheon.
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Published online: March 30, 2015
Published in issue: August 18, 2015
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Acknowledgments
This research was funded by National Science Foundation Grants 0936884 and 1317114 (to D.B.). A.P.M.W. appreciates support from the Deutsche Forschungsgemeinschaft (Grants EXC 1028 and WE 2231/8-2).
Notes
This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of Organelles,” held October 15–17, 2014, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. The complete program and video recordings of most presentations are available on the NAS website at www.nasonline.org/Symbioses.
This article is a PNAS Direct Submission. P.J.K. is a guest editor invited by the Editorial Board.
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Competing Interests
The authors declare no conflict of interest.
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