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Genome Biology and Evolution Advance Access published online on September 2, 2009
Genome Biology and Evolution, doi:10.1093/gbe/evp032
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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 Zhaxybayeva1,*,$, W. Ford Doolittle1, R. Thane Papke2 and J. Peter Gogarten2

1 Department of Biochemistry and Molecular Biology, Dalhousie University, 5850 College Street, Halifax, NS, B3H 1X5, Canada
2 Department of Molecular and Cell Biology, University of Connecticut, 91 North Eagleville Road, Storrs, CT 06269-3125 USA

* corresponding author, email: olga{at}environmentalproteomics.ca


  Abstract

Prochlorococcus is a genus of marine cyanobacteria characterized by small cell and genome size, an evolutionary trend towards low GC content, the possession of chlorophyll b, and the absence of phycobilisomes. While 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 scatterplots 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 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 a created a "highway of gene sharing" (Beiko et al. 2005, PNAS 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

Received July 25, 2009; Revised August 26, 2009; Accepted August 28, 2009

$ Current address: Environmental Proteomics NB, 22 Bickerton Ave., Sackville, NB, E4L 3M7, Canada


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