A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells

Abstract

Cyanobacteria are important contributors to primary production in the open oceans. Over the past decade, various photosynthesis-related genes have been found in viruses that infect cyanobacteria (cyanophages). Although photosystem II (PSII) genes are common in both cultured cyanophages and environmental samples , viral photosystem I (vPSI) genes have so far only been detected in environmental samples . Here, we have used a targeted strategy to isolate a cyanophage from the tropical Pacific Ocean that carries a PSI gene cassette with seven distinct PSI genes (psaJF, C, A, B, K, E, D) as well as two PSII genes (psbA, D). This cyanophage, P-TIM68, belongs to the T4-like myoviruses, has a prolate capsid, a long contractile tail and infects Prochlorococcus sp. strain MIT9515. Phage photosynthesis genes from both photosystems are expressed during infection, and the resultant proteins are incorporated into membranes of the infected host. Moreover, photosynthetic capacity in the cell is maintained throughout the infection cycle with enhancement of cyclic electron flow around PSI. Analysis of metagenomic data from the Tara Oceans expedition shows that phages carrying PSI gene cassettes are abundant in the tropical Pacific Ocean, composing up to 28% of T4-like cyanomyophages. They are also present in the tropical Indian and Atlantic Oceans. P-TIM68 populations, specifically, compose on average 22% of the PSI-gene-cassette carrying phages. Our results suggest that cyanophages carrying PSI and PSII genes are likely to maintain and even manipulate photosynthesis during infection of their Prochlorococcus hosts in the tropical oceans.

Integrated mobile genetic elements in Thaumarchaeota

“…For instance, multicopper oxidases, AmoC and nitrogen regulatory protein PII encoded by iMGE might modulate nitrogen metabolism, whereas UspA family proteins could boost the adaptation and survival of the host cells under various environmental stress conditions. The identification of functionally diverse metabolic and signalling genes in the thaumarcaheal iMGE parallels observations on the gene repertoires of some of the tailed bacterial viruses (Anantharaman et al ., ; Hurwitz and U'Ren, ; Roux et al ., ; Roitman et al ., ), in particular, cyanophages that carry photosystem genes and substantially contribute to the host metabolism (Sharon et al ., ; Thompson et al ., ; Fridman et al ., ). Taken together, these observations indicate that, at least, in the case of iMGEs with larger genomes, these elements should be considered more as symbionts of their hosts than simple genomic parasites or ‘junk DNA’.…”

Cyanophage MazG is a pyrophosphohydrolase but unable to hydrolyse magic spot nucleotides

“…This subversion of host metabolism is facilitated by the expression of cyanophage genes that appear to have a bacterial origin, so-called auxiliary metabolic genes (AMGs) (Breitbart et al, 2007). These include genes involved in photosynthesis (Mann et al, 2003;Lindell et al, 2005;Fridman et al, 2017) and photoprotection (Lindell et al, 2004;Millard et al, 2004;Sullivan et al, 2005;Roitman et al, 2018), pigment biosynthesis (Dammeyer et al, 2008), central carbon metabolism (Millard et al, 2009;Thompson et al, 2011), nucleotide biosynthesis (Enav et al, 2014), phosphorus metabolism (Sullivan et al, 2010;Zeng and Chisholm, 2012;Lin et al, 2016) and other stress responses (Sullivan et al, 2010;Crummett et al, 2016).…”

Bacterial Diversification in the Light of the Interactions with Phages: The Genetic Symbionts and Their Role in Ecological Speciation

“…From both angles, these processes can maintain the ecotype and sustain the emergence of new ecotypes while environmental conditions are changing (Figure 2). With that, bacteria-phage interactions modulate the biogeochemical cycles and ecosystem processes (e.g., photosynthesis; Fridman et al, 2017), thus ensuring that there is always a population that is most suited to use the available resources, even as resource abundance fluctuates.…”