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Cycles: dynamic phage-host relationships
- Phage-Host Interaction: an Ecological Perspective

Time series experiments revealed the seasonality in marine phage titers, demonstrating a dynamic relationship between phages and their bacterial hosts (8). In fact, at any given moment the marine phage titer is the net result from two opposing processes: synthesis of new phage particles due to ongoing lytic phage infections, which is balanced by phage decay. Sunlight UV was identified as the major destructive factor (69), causing up to 5% phage infectivity loss per hour for surface waters due to thymine dimer formation.

Repeat samples from a Norwegian fjord demonstrated seasonality in the viral titers, with a low in the cold winter season and a high in the summer. As a general rule, bacterioplankton produces greater amounts of phages under environmental conditions favoring fast bacterial growth and productivity. Other phage cycles occur on shorter time scales, as predicted by the "killing the winner populations" hypothesis. This concept states that phages expand on the fastest growing host population in the given ecological setting (54). The phage epidemic ceases when the diminished host population no longer supports phage replication. There is strong ecological evidence that some bloom collapse is in fact mediated by phage lysis: in the prealpine Lake of Constance, a transient increase in bacterial abundance was closely followed by peaks in the frequency of infected bacteria and then free phage (32) (Fig. 1B). Variability in the ocean was shown even over half-hour time intervals, probably reflecting synchronized infection cycles (8).

Cyclic phage development was also seen in other environments. Two types of Serratia phages were associated with the soil surrounding sugar beets: temperate Siphoviridae with a long latent period and big burst size and virulent Podoviridae with a short latent period and a small burst size. Over a 6-month observation period, the initially predominant siphovirus population changed to one dominated by the podovirus. Apparently, the two phages are adapted to two quite different niches in the rhizosphere, where the availability and physiological status of bacteria and plants changes with time (2). Some reports indicate that phage-host interaction can be quite complicated in the soil. In streptomycetes, spatial heterogeneity in phage-host interaction and temporal changes in phage susceptibility defined bacterial escape strategies from phage lysis. It was revealed that germinating spores were more susceptible to phage infection than hyphae of developed mycelia. Mature, resistant mycelia adsorb most of the Streptomyces-specific soil phages and thus protect younger, susceptible hyphae from infection (15).

Fluctuating phage titers are also a common observation in the dairy factory. This reflects the buildup and ensuing disappearance of phages specific for a starter strain imposed by the starter strain rotation system. Phage dynamics were also documented in a large intervention trial in a cheese factory (14) (Fig. 1A). One starter combination was replaced by a second that was insensitive to the resident phages of the factory. The intervention resulted in a nearly immediate disappearance of the resident phages. However, 5 to 7 days after the intervention, the first phages infecting the new starters were detected. Restriction enzyme analysis of the phage DNA traced the origin of the new phages to the rare phages in the raw milk samples delivered to the factory during the intervention period. Phage titers increased rapidly to the former levels, and starter rotation had to be reintroduced. Persistence of the phage in the absence of a propagating starter strain was not observed in the factory (unpublished observations).

In the human gut, it was reported that phage types and titers differed when healthy adults and patients suffering from traveler's diarrhea were compared (28). The former excreted low titers of lambda-like phages, while the latter yielded higher numbers of T4-like phages. This change in the phage population was suggested to reflect disturbances of the intestinal microflora during a bout of diarrhea.

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