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Home » Biology Articles » Ecology » Phage-Host Interaction: an Ecological Perspective » Numbers: phage titers in the biosphere

Numbers: phage titers in the biosphere
- Phage-Host Interaction: an Ecological Perspective

Just 14 years ago, a Norwegian group surprised the scientific community with a report on the high concentration of phage-like particles in coastal water and the ocean and even higher concentrations in lakes (5). In eutrophic estuarine water, bacteria are found at a density of 106 cells/ml and viruses with a concentration of 107 particles/ml. These concentrations are estimates that vary with the seasons and the geographical location. In addition, these figures refer to physical and not viable entities. A popular model postulates about 10 to 50 different bacterial species and 100 to 300 different phage strains (70) in this environment. The higher number of phage species was justified by the fact that each bacterial species may be infected by 10 phage species. As one would expect, the production and distribution of marine phages are determined by the productivity and density of the host bacterial populations. This relationship is expressed by the virus-to-bacterium ratio that is frequently at 10 to 1. For a comprehensive review on viruses in water and an extensive reference list see reference 68. Substantial theoretical and experimental research efforts were undertaken to determine the quantitative degree of virus-mediated bacterial mortality and to assess the ratio of phage lysis versus grazing of bacteria by protists and multicellular organisms. The greatest impact of phage lysis was seen in oligotrophic environments, and the ratio of lysis versus grazing changed with water depth both in the ocean and in lakes (66). To summarize the extensive literature, different approaches in various environments yielded a remarkably constant rate of virus-mediated bacterioplankton mortality of about 15% per day (61). The rate seems to be higher for heterotrophic bacteria than for the autotrophic cyanobacteria (61). Ecologically even more important is the profound effect of phages on the relative proportions of different bacterial species or strains in a community.

All these figures have important consequence for our biological view of the world. If phages outnumber bacteria in the ocean, phages are likely to be numerically the most prominent biological systems on earth, with an estimated population size of >=1030 phage particles. With these numbers, even rare phage-induced events manifest with high frequency. For example, transduction, the accidental packaging of bacterial host DNA into a phage particle, occurs under optimal laboratory conditions about once in every 108 phage infections. When calculated for the global marine phage population, it follows that gene transfer between organisms takes place about 20 million billion times per second in the oceans (16). The actual numbers will probably be lower due to smaller transduction efficiency and more rapid phage decay in the ocean than in the laboratory. If only a small part of this DNA is traveling between different bacterial species, gene transfer via marine phages opens up enormous possibilities for horizontal DNA transfer between bacteria.

High concentrations of phages are not restricted to the ocean water. Counts of up to 109 phage per gram of marine sediment were recorded with bacterial counts higher than in the waters described above (21). Terrestrial ecosystems, e.g., soil associated with plant roots in sugar beet fields, revealed 107 viruses per gram by using transmission electron microscopy (1). Not all viruses will be viable, but hybridization experiments with Serratia and Pseudomonas spp. from the soil showed that about 5% of the bacteria are actually phage infected.

There is a dictum that phages are found where bacteria thrive. Thus, we should not be surprised that phages are found on us (skin) and within us (oral cavity, gut). In a survey of stool samples from 600 healthy adults, 34% of the subjects demonstrated coliphages (but only 1% showed high amounts) (28). Most of them were classified as temperate phages related to phage lambda. Ruminants that rely heavily on bacteria for cellulose digestion show intestinal phage concentrations in excess of 107 phages per gram of feces. Stool phages were mainly explored for their potential to trace fecal contamination in the environment and to monitor the intrusion of polluted surface waters into groundwater.

Phages are also present in the food we eat. Many food products from our daily life are the result of fermentation processes by lactic acid bacteria. Cheese factories using Lactococcus lactis can be contaminated with high levels of phages; one study reported up to 109 phage per ml of whey and up to 105 phage per m3 in the air (48). When the phage titers exceeded 103 PFU/ml, the yogurt fermentation process was delayed and came to a stop at higher phage titers, leading to important economical losses (unpublished observations).

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