Diel Infection of a Cyanobacterium by a Contractile Bacteriophage

Abstract

Light was found to strongly influence the infection of a freshwater cyanobacterium (Synechococcus elongatus PCC 7942) by a contractile DNA phage named AS-1. Phage progeny production was correlated with the amount of light in the laboratory and occurred in a diel pattern under natural light. At least one effect of light on AS-1 infection is at the level of adsorption.Viruses are present in marine and freshwater systems at more than 10 7 particles per milliliter (4,18). This large number argues strongly for an important role in global biological and geochemical processes, including the recycling of nutrient stores due to virus-induced lysis (4,6,13,20). In addition, phylogenetic analysis has revealed that viruses in aquatic ecosystems are genetically diverse, suggesting that they are under significant selection pressure, perhaps in response to host defense systems and/or variations in the environment (22). Understanding how environmental factors and/or host genetics affect the success of viral infection is therefore relevant to the understanding of aquatic ecosystems.A previously characterized contractile DNA phage of Synechococcus elongatus named AS-1 is a member of the family Myoviridae, which includes the well-characterized T-even phages (11,(14)(15)(16) (Fig. 1A). AS-1 infects the well-characterized freshwater obligate phototroph Synechococcus elongatus PCC 7942 (14). A key feature of S. elongatus biology is that its gene expression is regulated by an intrinsic ϳ24-h circadian clock (5,7,8). The products of three key genes, kaiA, kaiB, and kaiC, are required for maintaining the normal gene expression rhythm (7,8). Deletion of any of these three genes will result in a loss of rhythmicity but will not significantly affect growth rates (5). We were initially interested in examining whether mutations in circadian rhythm regulators of S. elongatus would affect AS-1 infection. We found that deletions in the genes that regulate S. elongatus circadian rhythm had only minor effects on AS-1 progeny production, whereas light had a profound influence on the AS-1 infection process. MATERIALS AND METHODSS. elongatus strain AMC541 is the parental strain for the circadian mutants. Strains AMC702, AMC703, and AMC704 have deletions in the kaiA, kaiB, and kaiC genes, respectively. Additional genetic information concerning the strains used can be found in the report of Ditty et al. (5). Cultures were usually grown under constant illumination at 45 mol photons m Ϫ2 s Ϫ1 in a modified BG-11 medium (2). Light intensity was measured with a LiCor luminometer. The original preparation of AS-1 was obtained from the American Type Culture Collection. A stock of at least 10 9 phage per ml was prepared by infecting S. elongatus grown in the presence of light for more than 18 h, followed by two clarifications of the supernatant of the culture lysate by centrifugation. The clarified lysate was stored at 4°C with a drop of chloroform. As previously determined by Safferman et al. (14), the lysate was stable for a minimum of several weeks at 4°C...

Impairment of O-antigen production confers resistance to grazing in a model amoeba–cyanobacterium predator–prey system

“…Although the O-antigen of Anacystis nidulans KM, an isolate likely to be essentially identical to S. elongatus PCC 7942, was shown to structurally and chemically resemble that of E. coli O8 (49), the genes involved in O-antigen synthesis and transport in S. elongatus had not been previously identified and characterized. Our discovery that S. elongatus uses a Wzm/Wzt O-antigen transport system homologous to that of E. coli O8 and O9 is consistent with the O-antigen structure of A. nidulans KM, whose lipopolysaccharide is involved in adsorption of the cyanophage AS-1 (50), which also infects S. elongatus PCC 7942 (51). Whereas the dominant mechanism of O-antigen production in enterics is the Wzx/Wzy flippase pathway (52), the Wzm/Wzt system appears to predominate among the cyanobacteria.…”

Comparison of lysogeny (prophage induction) in heterotrophic bacterial and Synechococcus populations in the Gulf of Mexico and Mississippi river plume

“…The recent discovery that many lytic cyanophages carry host-like photosynthesis genes indicates that the lytic cycle of their associated cyanophages is also light dependent (Lindell et al, 2005;Sullivan et al, 2006). Additionally, it has been verified for cyanophages S-PM2, AS-1 and AS-1M that phage adsorption is light dependent (Sherman, 1976;Jia and Mann, 2005;Kao et al, 2005). It has been hypothesized that a wave of phage adsorption following dawn could lead to a release of progeny phage later in the day (Clokie and Mann, 2006).…”

Genomic and Biological Analysis of Phage Xfas53 and Related Prophages of Xylella fastidiosa

“…There are conditions under which a reduced adsorption rate might be beneficial even to planktonic bacteria. Cyanophage AS-1, for example, exhibits light-dependent changes in adsorption kinetics (33). An interesting model was proposed suggesting that the lack of adsorption in the dark would result in phage remaining as free particles during the period when the host cells are not metabolically active, reducing the chances of the phage being grazed by nocturnal predators of bacteria (17).…”