A Hitchhiker's Guide to the Ocean

by Roberto

 

When it comes to horizontal gene transfer (HGT) and its key role in microbial evolution, we are great fans of it here at STC (read, for the example, Christoph's in-depth three-part series on the subject). Plasmids, autonomously replicating extrachromosomal elements, have long been recognized as important HGT agents. A striking early example of this was the discovery – some sixty years ago – of the very rapid and efficient plasmid-mediated transfer of multiple antibiotic resistance genes in clinical settings. This classic paper by Watanabe and Fukasawa makes for great reading on the subject.
 

Several features of plasmids render them particularly good vectors to mediate rapid and efficient HGT. First, they don't have great constraints on the number and types of genes that they carry. Couple to that the fact that they can gain new genes by homologous and non-homologous (for example, by transposition), you can then imagine that plasmids could, in theory, harbor almost any number and type of genes. And, of course, their key attribute is that they can move from one cell to another via conjugation. Almost all naturally occurring plasmids have this feature. (That is not usually the case of those artificial constructs that you might treasure as your favorite cloning vector.) Regarding their ability to move from cell to cell, plasmids come in two flavors. Some are said to be "conjugative" because they harbor all the genes required to form the apparatus that mediates plasmid transfer. But many non-conjugative plasmids are said to "mobilizable." These carry a few genes - the mobility genes - that allow them to be transferred from cell to cell when the cell also contains a conjugative transfer. Hitchhikers of sorts… So now you know where I was headed with the title. This is the story of one such hitchhiker plasmid.
 

(click to enlarge)
Figure 1. Biogeography of pLA6_12-like plasmids. Samp­ling locations of Roseobacter group isolates are shown in squares. Locations where metagenomes have been obtained are shown in circles and triangles. pLA6_12-like plasmids were found exclusively in marine envi­ronments, but scattered across the world. Black tri­angles represent metagenome frag­ments, which enco­de pLA6_12-like repL genes, but are too incomplete to allow conclusions on the respective integration casset­te. Source

The role of plasmids in transfer of antibiotic resistance genes in the clinical setting is very clear. But how often and how widely do plasmids play similar gene transfer roles in environmental settings? The extent of how far, phylogenetically and physically, plasmids transfer on Earth has not been addressed much. At least not until recently. In an exciting PNAS paper by Jörn Petersen and colleagues, some surprising results addressing this question are described. During the genome sequencing of a new bacterium, a methylotrophic Roseobacter isolated from the coastal seawater from the United Kingdom (Marinibacterium anthonyi strain La 6), the authors identified a mobilizable plasmid – pLA6_12 – of 7,053 base pairs. This number is significant because they then realized that two other isolates, from the very distant Indian Ocean, contained plasmids of absolutely identical sequence, that is, 100% identity! Importantly, the two other plasmids were not only geographically distant, they were found in hosts that are phylogenetically distant: Roseovarius indicus and Celeribacter indicus. The authors state: "This is the only known instance where actual nucleotide identity, and not only high plasmid synteny, has been observed for extrachromosomal replicons in environmental organisms of distinct genera."  And, importantly, they rightly speculate: "This likely reflects very recent widespread HGT events."
 

Based on these results the authors proceeded to query metagenomic databases for the replication components of the plasmid, using a 95% sequence identity cut-off. They found sequences of this replicon distributed across all of Earth's oceans! Interestingly, they found that aside from the highly conserved replication, stability and mobility genes, the plasmids can harbor a variety of "cargo" genes, generally encoding functions which, in the words of the authors "confer resistance to toxins and xenobiotics, which might reflect rapid adaptations to the respective pollutants in marine habitats." So there you have it, a hitchhiker plasmid that appears to be moving genes around across remarkably large distances in the Earth's oceans (especially relative to the size of a bacterium) and providing evolutionary adaptive functions in response to human's tendency to pollute the planet.