Why do marine cyanophages carry metabolic genes from their hosts?

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The genomic content and context of auxiliary metabolic genes (AMGs) informs their adaptive significance

Text by Lisa Crummett

Auxiliary metabolic genes (AMGs) are host-derived genes carried by bacteriophages that support key steps in host metabolism during infection. AMGs have been found in many types of bacteriophages, including those that infect marine cyanobacteria (cyanophages). For instance, all cyanophages from the family Myoviridae were thought to encode the psbA gene. This photosynthesis gene is expressed during phage infection, suggesting that phages contribute to photosynthesis before killing the host cell.  Other phage-encoded AMGs are also presumed to increase phage fitness by altering metabolic pathways that enhance phage reproduction such as nucleic acid biosynthesis.

Over the past 15 years, the Marston and Martiny labs have isolated cyanophages from the Atlantic and Pacific coasts of North America. This collection now includes over 10,000 isolates. We decided to use this collection to investigate the presence of various AMGs across cyanophage genomes and how this might relate to their location of isolation and genetic relatedness among phages.

To do this, we sequenced the genomes of some of our cyanophages and compared them to other publically available genomes. We found that uncommon AMGs (those that were present in only a few genomes) also moved around more in the genomes. In contrast, common AMGs (present in most genomes) tended to be present in the same genomic location. This result suggests that rare AMGs may confer a fitness advantage only under particular environments or in the presence of particular hosts; therefore, these AMGs may be transmitted horizontally more often than common AMGs.

A surprise in the genomes was that one of the cyanophages (and all the isolates within this taxon) lacked psbA (and many other common AMGs). This raises the question: does this phage have a different life strategy than those who carry such photosynthesis genes? One intriguing possibility is that it might infect heterotrophic bacteria in addition to cyanobacteria.

One of the problems we faced in analyzing our data was how to compare the genomic context of AMGs in an objective way. For instance, we wanted to compare our results to previous studies that observed that AMGs tended to be present in hypervariable regions of the cyanophage genomes. However, tracking the location of over 30 genes across 60 divergent genomes became difficult. Therefore we developed a method to identify stretches of conserved genomic content and then define the location of the AMGs within those conserved “blocks.”

figure

Figure legend

Relationship between the fraction of genomes containing an AMG and the LCB-distribution index (LDI). The LDI is calculated as the number of discrete LCBs in which an AMG is found divided by the frequency of the AMG across the 60 genomes; the more variable the genomic location, the closer the LDI is to one. PyrE is greater than one because a breakpoint between two LCBs intersected the gene and thus it was assigned to two distinct LCBs. The grey lines indicate 2nd order polynomial fits to each of 100 simulated datasets (open circles). The dashed black line is the best polynomial fit to the actual data.

Introducing the authors

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Pictured left is Dr. Lisa T. Crummett, Assistant Professor of Biology, Soka University of America, Aliso Viejo, California, USA. Pictured right is Dr. Richard J. Puxty, Research Fellow, School of Life Sciences, University of Warwick, UK.

About the research

The genomic content and context of auxiliary metabolic genes in marine cyanomyoviruses
Lisa T. Crummett, Richard J. Puxty, Claudia Weihe, Marcia F. Marston, Jennifer B.H. Martiny
Virology, Volume 499, December 2016, Pages 219–229