Patterns and Implications of Gene Gain and Loss in the Evolution of Prochlorococcus

Abstract

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.

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

“…hlis were originally identified as genes that played a role in protecting cells from light shock (Funk and Vermaas, 1999;He et al, 2001;Bhaya et al, 2002), and are now known to respond to a variety of stresses in Prochlorococcus (Tolonen et al, 2006;Lindell et al, 2007;Thompson et al, 2011; Bagby and Chisholm, 2015). hlis are found in all Prochlorococcus genomes, but NATL2A is notable for having a much larger suite of hlis than many other Prochlorococcus (Coleman and Chisholm, 2007;Kettler et al, 2007;Berta-Thompson, 2015), which may be related to the ability of this clade of low-light adapted Prochlorococcus to withstand transient exposure to high light intensities (Malmstrom et al, 2010). All 12 of these hli transcripts decreased in relative abundance in co-culture conditions, suggesting that the Alteromonas may have mitigated some form of stress in the culture, such as oxidative stress (Morris et al, 2011).…”

“…Prochlorococcus NATL2A contains the complete pathway for synthesizing vitamin B 12 (Kettler et al, 2007). Many marine microbes are known to be vitamin B 12 auxotrophs as they require this cofactor for essential functions such as methionine biosynthesis, yet lack the capability to make it themselves (Croft et al, 2005;Sañudo-Wilhelmy et al, 2013); this has led to the suggestion that exchange of vitamin B 12 may have an important ecological role in the marine environment (Kazamia et al, 2012;Bertrand et al, 2015).…”

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…Gene families encoding short peptides form a major part of the response of MIT9313 to co-culture During the analysis of the transcriptional changes in co-cultures, we noticed two peculiarities about the response of MIT9313 as it was stressed by an inhibitive dose of Alteromonas HOT1A3 (9313+ 1A3): (a) much of the transcriptional response seemed to be clustered around three regions along the genome, which were also associated with the presence of many newly acquired genes (Figure 2d) (Kettler et al, 2007;Thompson et al, 2011). (b) Many of the genes that were differentially regulated had a short predicted protein product (~100 amino acids long, Figure 4a, Supplementary Figure S3).…”

“…A Bayesian tree constructed from protein sequences is shown, with circles on the nodes denoting 40.5 probability. Clade assignment and color coding are according to Kettler et al (2007). Prochlorococcus w7 is a sequenced genome from a single cell sorted from an environmental sample (Malmstrom et al, 2012).…”

The Yfr2 ncRNA family, a group of abundant RNA molecules widely conserved in cyanobacteria

“…At present there are 24 genome sequences for marine picocyanobacteria available in the public domain, 12 of the genus Prochlorococcus and 12 of the genus Synechococcus. 5,6 …”