Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA)
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 (us...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-01-01
|
| Series: | Frontiers in Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.00045/full |
| _version_ | 1819131961459867648 |
|---|---|
| author | Patricia Sánchez-Baracaldo Giorgio Bianchini Andrea Di Cesare Andrea Di Cesare Cristiana Callieri Nathan A. M. Chrismas Nathan A. M. Chrismas |
| author_facet | Patricia Sánchez-Baracaldo Giorgio Bianchini Andrea Di Cesare Andrea Di Cesare Cristiana Callieri Nathan A. M. Chrismas Nathan A. M. Chrismas |
| author_sort | Patricia Sánchez-Baracaldo |
| collection | DOAJ |
| description | 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 Syn/Pro clade, Sub-Cluster 5.3, includes marine and freshwater strains. Relaxed molecular clock (SSU, LSU) analyses show that while ancestors of the Syn/Pro clade date as far back as the end of the Pre-Cambrian, modern crown groups evolved during the 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, appear 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 marine and non-marine 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 Syn/Pro clade and S. spongiarum. During the diversification of Synechococcus lineages, losses of mpeBA genes may explain the emergence of pigment cluster Types I, II, IIB, and III in both marine and non-marine habitats, with few lateral gene transfer events in specific taxa. |
| first_indexed | 2024-12-22T09:23:49Z |
| format | Article |
| id | doaj.art-e79b54e2c0b04fb28426f0b86bda144e |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-22T09:23:49Z |
| publishDate | 2019-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-e79b54e2c0b04fb28426f0b86bda144e2022-12-21T18:31:08ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-01-011010.3389/fmicb.2019.00045427258Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA)Patricia Sánchez-Baracaldo0Giorgio Bianchini1Andrea Di Cesare2Andrea Di Cesare3Cristiana Callieri4Nathan A. M. Chrismas5Nathan A. M. Chrismas6School of Geographical Sciences, University of Bristol, Bristol, United KingdomSchool of Geographical Sciences, University of Bristol, Bristol, United KingdomInstitute of Ecosystem Study–Consiglio Nazionale delle Ricerche, Verbania, ItalyDepartment of Earth, Environment and Life Sciences, University of Genoa, Genoa, ItalyInstitute of Ecosystem Study–Consiglio Nazionale delle Ricerche, Verbania, ItalySchool of Geographical Sciences, University of Bristol, Bristol, United KingdomThe Marine Biological Association of the United Kingdom, The Laboratory, Citadel Hill, Plymouth, United KingdomMarine 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 Syn/Pro clade, Sub-Cluster 5.3, includes marine and freshwater strains. Relaxed molecular clock (SSU, LSU) analyses show that while ancestors of the Syn/Pro clade date as far back as the end of the Pre-Cambrian, modern crown groups evolved during the 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, appear 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 marine and non-marine 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 Syn/Pro clade and S. spongiarum. During the diversification of Synechococcus lineages, losses of mpeBA genes may explain the emergence of pigment cluster Types I, II, IIB, and III in both marine and non-marine habitats, with few lateral gene transfer events in specific taxa.https://www.frontiersin.org/article/10.3389/fmicb.2019.00045/fullpicocyanobacteriaSynechococcusCyanobiumphycobilisomesphylogenomicscomparative genomics |
| spellingShingle | Patricia Sánchez-Baracaldo Giorgio Bianchini Andrea Di Cesare Andrea Di Cesare Cristiana Callieri Nathan A. M. Chrismas Nathan A. M. Chrismas Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA) Frontiers in Microbiology picocyanobacteria Synechococcus Cyanobium phycobilisomes phylogenomics comparative genomics |
| title | Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA) |
| title_full | Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA) |
| title_fullStr | Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA) |
| title_full_unstemmed | Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA) |
| title_short | Insights Into the Evolution of Picocyanobacteria and Phycoerythrin Genes (mpeBA and cpeBA) |
| title_sort | insights into the evolution of picocyanobacteria and phycoerythrin genes mpeba and cpeba |
| topic | picocyanobacteria Synechococcus Cyanobium phycobilisomes phylogenomics comparative genomics |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.00045/full |
| work_keys_str_mv | AT patriciasanchezbaracaldo insightsintotheevolutionofpicocyanobacteriaandphycoerythringenesmpebaandcpeba AT giorgiobianchini insightsintotheevolutionofpicocyanobacteriaandphycoerythringenesmpebaandcpeba AT andreadicesare insightsintotheevolutionofpicocyanobacteriaandphycoerythringenesmpebaandcpeba AT andreadicesare insightsintotheevolutionofpicocyanobacteriaandphycoerythringenesmpebaandcpeba AT cristianacallieri insightsintotheevolutionofpicocyanobacteriaandphycoerythringenesmpebaandcpeba AT nathanamchrismas insightsintotheevolutionofpicocyanobacteriaandphycoerythringenesmpebaandcpeba AT nathanamchrismas insightsintotheevolutionofpicocyanobacteriaandphycoerythringenesmpebaandcpeba |