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Front. Microbiol. | doi: 10.3389/fmicb.2019.00045

Insights into the evolution of picocyanobacteria and phycoerythrin genes (mpeBA and cpeBA)

  • 1University of Bristol, United Kingdom
  • 2School of Geographical Sciences, Faculty of Science, University of Bristol, United Kingdom
  • 3University College, Bristol, United Kingdom
  • 4Istituto per lo studio degli ecosistemi (ISE), Italy
  • 5Marine Biological Association of the United Kingdom, United Kingdom

Marine picocyanobacteria, Prochlorococcus and Synechococcus, substantially contribute to marine primary production and have been the subject of extensive ecological and genomic studies. Little is known about their close relatives from freshwater and non-marine environments. Phylogenomic analyses (using 136 proteins) provide strong support for the monophyly of a clade of non-marine picocyanobacteria consisting of Cyanobium, Synechococcus and marine Sub-cluster 5.2; this clade itself is sister to marine Synechococcus and Prochlorococcus. The most basal lineage within the SynPro clade, Sub-Cluster 5.3, includes marine and freshwater strains. Relaxed molecular clock (SSU, LSU) analyses show that while ancestors of the SynPro clade date as far back at the end of Pre-Cambrian, modern crown groups evolved during Carboniferous and Triassic. Comparative genomic analyses reveal novel gene cluster arrangements involved in phycobilisome (PBS) metabolism in freshwater strains. Whilst PBS genes in marine Synechococcus are mostly found in one type of phycoerythrin (PE) rich gene cluster (Type III), strains from non-marine habitats, so far, appeared to be more diverse both in terms of pigment content and gene arrangement, likely reflecting a wider range of habitats. Our phylogenetic analyses show that the PE genes (mpeBA) evolved via a duplication of the cpeBA genes in an ancestor of the picocyanobacteria and of the symbiotic strains Synechococcus spongiarum. A ‘primitive’ Type III-like ancestor containing (cpeBA and mpeBA) had thus evolved prior to the divergence of the SynPro clade and S. spongiarum. During the diversification of Synechococcus lineages, losses of mpeBA genes may explain the emergence of pigment cluster Types II, IIB and III in both marine and non-marine habitats, with few Lateral Gene Transfer events in specific taxa.

Keywords: picocyanobacteria, Synechoccocus, Cyanobium, Phycobilisomes, Phycoerythrin

Received: 27 Sep 2018; Accepted: 11 Jan 2019.

Edited by:

Petr Dvorak, Palacký University, Olomouc, Czechia

Reviewed by:

Vera Tai, University of Western Ontario, Canada
Jeffrey Morris, University of Alabama at Birmingham, United States  

Copyright: © 2019 Sanchez-Baracaldo, Bianchini, Di Cesare, Callieri and Chrismas. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Patricia Sanchez-Baracaldo, University of Bristol, Bristol, United Kingdom, p.sanchez-baracaldo@bristol.ac.uk