Format

Send to

Choose Destination
Proc Natl Acad Sci U S A. 2015 Aug 18;112(33):10208-15. doi: 10.1073/pnas.1421375112. Epub 2015 Mar 30.

Metabolic connectivity as a driver of host and endosymbiont integration.

Author information

1
Department of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ 08901; and.
2
Institut für Biochemie der Pflanzen, Cluster of Excellence on Plant Sciences, Heinrich-Heine Universität, D-40225 Düsseldorf, Germany.
3
Institut für Biochemie der Pflanzen, Cluster of Excellence on Plant Sciences, Heinrich-Heine Universität, D-40225 Düsseldorf, Germany andreas.weber@uni-duesseldorf.de debash.bhattacharya@gmail.com.
4
Department of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ 08901; and andreas.weber@uni-duesseldorf.de debash.bhattacharya@gmail.com.

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.

KEYWORDS:

Arabidopsis thaliana; endosymbiosis; evolution; network analysis; symbiont integration

PMID:
25825767
PMCID:
PMC4547263
DOI:
10.1073/pnas.1421375112
[Indexed for MEDLINE]
Free PMC Article

Supplemental Content

Full text links

Icon for HighWire Icon for PubMed Central
Loading ...
Support Center