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Genome Biology and Evolution Advance Access originally published online on September 2, 2009
Genome Biology and Evolution (2009) Vol. 2009:325; doi:10.1093/gbe/evp032 published on September 23, 2009
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© 2009 The Authors
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Intertwined Evolutionary Histories of Marine Synechococcus and Prochlorococcus marinus

Olga Zhaxybayeva*,1, W. Ford Doolittle*, R. Thane Papke{dagger} and J. Peter Gogarten{dagger}

* Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada
{dagger} Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT

E-mail: olga{at}environmentalproteomics.ca.


  Abstract

Prochlorococcus is a genus of marine cyanobacteria characterized by small cell and genome size, an evolutionary trend toward low GC content, the possession of chlorophyll b, and the absence of phycobilisomes. Whereas many shared derived characters define Prochlorococcus as a clade, many genome-based analyses recover them as paraphyletic, with some low-light adapted Prochlorococcus spp. grouping with marine Synechococcus. Here, we use 18 Prochlorococcus and marine Synechococcus genomes to analyze gene flow within and between these taxa. We introduce embedded quartet scatter plots as a tool to screen for genes whose phylogeny agrees or conflicts with the plurality phylogenetic signal, with accepted taxonomy and naming, with GC content, and with the ecological adaptation to high and low light intensities. We find that most gene families support high-light adapted Prochlorococcus spp. as a monophyletic clade and low-light adapted Prochlorococcus sp. as a paraphyletic group. But we also detect 16 gene families that were transferred between high-light adapted and low-light adapted Prochlorococcus sp. and 495 gene families, including 19 ribosomal proteins, that do not cluster designated Prochlorococcus and Synechococcus strains in the expected manner. To explain the observed data, we propose that frequent gene transfer between marine Synechococcus spp. and low-light adapted Prochlorococcus spp. has created a "highway of gene sharing" (Beiko RG, Harlow TJ, Ragan MA. 2005. Highways of gene sharing in prokaryotes. Proc Natl Acad Sci USA. 102:14332–14337) that tends to erode genus boundaries without erasing the Prochlorococcus-specific ecological adaptations.

Keywords: marine cyanobacteria, horizontal gene transfer, introgression, quartet decomposition, supertree, genome evolution

Accepted August 28, 2009

1 Current address: Environmental Proteomics NB, 22 Bickerton Avenue, Sackville, New Brunswick E4L 3M7, Canada

Eugene Koonin, Associate Editor


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