Patterns and implications of gene gain and loss in the evolution of Prochlorococcus.
Prochlorococcus is a marine cyanobacterium that numerically dominates the mid-latitude oceans and is the smallest known oxygenic phototroph. Numerous isolates from diverse areas of the world's oceans have been studied and shown to be physiologically and genetically distinct. All isolates descri...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2007-12-01
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| Series: | PLoS Genetics |
| Online Access: | http://europepmc.org/articles/PMC2151091?pdf=render |
| _version_ | 1828324961820868608 |
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| author | Gregory C Kettler Adam C Martiny Katherine Huang Jeremy Zucker Maureen L Coleman Sebastien Rodrigue Feng Chen Alla Lapidus Steven Ferriera Justin Johnson Claudia Steglich George M Church Paul Richardson Sallie W Chisholm |
| author_facet | Gregory C Kettler Adam C Martiny Katherine Huang Jeremy Zucker Maureen L Coleman Sebastien Rodrigue Feng Chen Alla Lapidus Steven Ferriera Justin Johnson Claudia Steglich George M Church Paul Richardson Sallie W Chisholm |
| author_sort | Gregory C Kettler |
| collection | DOAJ |
| description | Prochlorococcus is a marine cyanobacterium that numerically dominates the mid-latitude oceans and is the smallest known oxygenic phototroph. Numerous isolates from diverse areas of the world's oceans have been studied and shown to be physiologically and genetically distinct. All isolates described thus far can be assigned to either a tightly clustered high-light (HL)-adapted clade, or a more divergent low-light (LL)-adapted group. The 16S rRNA sequences of the entire Prochlorococcus group differ by at most 3%, and the four initially published genomes revealed patterns of genetic differentiation that help explain physiological differences among the isolates. Here we describe the genomes of eight newly sequenced isolates and combine them with the first four genomes for a comprehensive analysis of the core (shared by all isolates) and flexible genes of the Prochlorococcus group, and the patterns of loss and gain of the flexible genes over the course of evolution. There are 1,273 genes that represent the core shared by all 12 genomes. They are apparently sufficient, according to metabolic reconstruction, to encode a functional cell. We describe a phylogeny for all 12 isolates by subjecting their complete proteomes to three different phylogenetic analyses. For each non-core gene, we used a maximum parsimony method to estimate which ancestor likely first acquired or lost each gene. Many of the genetic differences among isolates, especially for genes involved in outer membrane synthesis and nutrient transport, are found within the same clade. Nevertheless, we identified some genes defining HL and LL ecotypes, and clades within these broad ecotypes, helping to demonstrate the basis of HL and LL adaptations in Prochlorococcus. Furthermore, our estimates of gene gain events allow us to identify highly variable genomic islands that are not apparent through simple pairwise comparisons. These results emphasize the functional roles, especially those connected to outer membrane synthesis and transport that dominate the flexible genome and set it apart from the core. Besides identifying islands and demonstrating their role throughout the history of Prochlorococcus, reconstruction of past gene gains and losses shows that much of the variability exists at the "leaves of the tree," between the most closely related strains. Finally, the identification of core and flexible genes from this 12-genome comparison is largely consistent with the relative frequency of Prochlorococcus genes found in global ocean metagenomic databases, further closing the gap between our understanding of these organisms in the lab and the wild. |
| first_indexed | 2024-04-13T19:15:09Z |
| format | Article |
| id | doaj.art-dfcec434a7a7454b92909dff4d23430b |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-04-13T19:15:09Z |
| publishDate | 2007-12-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-dfcec434a7a7454b92909dff4d23430b2022-12-22T02:33:43ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042007-12-01312e23110.1371/journal.pgen.0030231Patterns and implications of gene gain and loss in the evolution of Prochlorococcus.Gregory C KettlerAdam C MartinyKatherine HuangJeremy ZuckerMaureen L ColemanSebastien RodrigueFeng ChenAlla LapidusSteven FerrieraJustin JohnsonClaudia SteglichGeorge M ChurchPaul RichardsonSallie W ChisholmProchlorococcus is a marine cyanobacterium that numerically dominates the mid-latitude oceans and is the smallest known oxygenic phototroph. Numerous isolates from diverse areas of the world's oceans have been studied and shown to be physiologically and genetically distinct. All isolates described thus far can be assigned to either a tightly clustered high-light (HL)-adapted clade, or a more divergent low-light (LL)-adapted group. The 16S rRNA sequences of the entire Prochlorococcus group differ by at most 3%, and the four initially published genomes revealed patterns of genetic differentiation that help explain physiological differences among the isolates. Here we describe the genomes of eight newly sequenced isolates and combine them with the first four genomes for a comprehensive analysis of the core (shared by all isolates) and flexible genes of the Prochlorococcus group, and the patterns of loss and gain of the flexible genes over the course of evolution. There are 1,273 genes that represent the core shared by all 12 genomes. They are apparently sufficient, according to metabolic reconstruction, to encode a functional cell. We describe a phylogeny for all 12 isolates by subjecting their complete proteomes to three different phylogenetic analyses. For each non-core gene, we used a maximum parsimony method to estimate which ancestor likely first acquired or lost each gene. Many of the genetic differences among isolates, especially for genes involved in outer membrane synthesis and nutrient transport, are found within the same clade. Nevertheless, we identified some genes defining HL and LL ecotypes, and clades within these broad ecotypes, helping to demonstrate the basis of HL and LL adaptations in Prochlorococcus. Furthermore, our estimates of gene gain events allow us to identify highly variable genomic islands that are not apparent through simple pairwise comparisons. These results emphasize the functional roles, especially those connected to outer membrane synthesis and transport that dominate the flexible genome and set it apart from the core. Besides identifying islands and demonstrating their role throughout the history of Prochlorococcus, reconstruction of past gene gains and losses shows that much of the variability exists at the "leaves of the tree," between the most closely related strains. Finally, the identification of core and flexible genes from this 12-genome comparison is largely consistent with the relative frequency of Prochlorococcus genes found in global ocean metagenomic databases, further closing the gap between our understanding of these organisms in the lab and the wild.http://europepmc.org/articles/PMC2151091?pdf=render |
| spellingShingle | Gregory C Kettler Adam C Martiny Katherine Huang Jeremy Zucker Maureen L Coleman Sebastien Rodrigue Feng Chen Alla Lapidus Steven Ferriera Justin Johnson Claudia Steglich George M Church Paul Richardson Sallie W Chisholm Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genetics |
| title | Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. |
| title_full | Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. |
| title_fullStr | Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. |
| title_full_unstemmed | Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. |
| title_short | Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. |
| title_sort | patterns and implications of gene gain and loss in the evolution of prochlorococcus |
| url | http://europepmc.org/articles/PMC2151091?pdf=render |
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