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Biology Articles » Ecology » Phage-Host Interaction: an Ecological Perspective » Polyvalency: finding the right cell

Polyvalency: finding the right cell
- Phage-Host Interaction: an Ecological Perspective

In near coastal water, the bacterial population consists of 106 cells per ml distributed over 100 different bacterial host species (68). Less than 104 cells per ml therefore constitute the average target population for a species-specific phage. Streptococcus thermophilus phages are found with titers of 200 infectious phages per ml of raw milk (14), while its target cell is only detected in raw milk after enrichment. How can phage infection cycles be maintained under these conditions? Laboratory experiments with three phages, including T4, showed that phage production did not occur below 104 cells/ml (67). Statistical analysis and back-calculations in natural marine environments predicted 105 cells/ml as minimal bacterioplankton concentrations for successful virus production. However, some marine viruses replicated efficiently down to 103 specific host cells/ml (62). The determination of the variations of host cell concentration over time allowed the approximation that cyanophage replication still occurred when the host cell concentration fell to 102 cells/ml (65).

Broad-host-range (polyvalent) phages could be a solution to this dilemma. Indeed, some observations suggest that phages isolated from nutrient-poor marine environments showed a trend towards increased polyvalency, possibly representing an adaptation to low host cell concentrations.

For most phages investigated in the laboratory, host species specificity is the rule. The polyvalent phages infecting different genera in the Enterobacteriaceae must be regarded with some caution because this family is such a closely related bacterial group. Even data on marine phages indicate that most of them are host species specific, many even demonstrate strain specificity. Polyvalence was more prevalent in cyanophages, but fluorescence-labeled cyanophages (33) demonstrated that they attached specifically only to their host and not other bacteria of the natural consortium. Data from the ocean showed that polyvalency was correlated with phage morphology. Phages isolated from high-light-adapted Prochlorococcus hosts yielded exclusively Podoviridae that were strain specific (60). In contrast, low-light-adapted Prochlorococcus hosts yielded Myoviridae that also infected Synechococcus spp., a phylogenetically related cyanobacterium. Similarly, Synechococcus-infecting Myoviridae also cross-infected Prochlorococcus spp., lending some support to the polyvalency concept in the marine environment. Also, in other environments, Myoviridae showed a broader host range than Siphoviridae and Podoviridae.

Polyvalency was not described in dairy phages: the analysis of hundreds of phage isolates from cheese factories showed a very narrow host range. We are only aware of exceptions for Lactobacillus phages appearing in sauerkraut fermentation: one phage isolate could infect two ecologically related Lactobacillus species (42). Furthermore, about 30% of lactobacilli constituting the major commensals in the vagina of healthy women were lysogenic. Many lysogens could be induced by mitomycin C, and some phages could infect up to five different Lactobacillus species, which dominate the vaginal flora (36).

Even if polyvalency is not the rule, many phages have developed efficient methods to change their host range by elegant genetic tricks. A classical case is phage Mu, containing a recombinase that inverses the orientation of the receptor-interacting gene leading to the synthesis of a new receptor recognition specificity. A coliphage possessed two different tail fiber proteins and showed the combined host range of phages containing either one or the other tail gene (56). The similarities in the tail fiber genes of coliphages belonging to different phage families (P2, T4, lambda) provide evidence that illegitimate recombination resulting in domain exchanges occurs at previously unappreciated levels (31). Similarly, phages infecting lactic streptococci can alter their host range by exchanging variable domains flanked by conserved collagen-like repeats that serve as target sites for homologous recombination (23). A fundamentally different method of host range changes was recently described for Bordetella phages (40). At one genome end, the mtd (major tropism determinant) gene encodes the phage protein responsible for host cell recognition. Its C-terminal end varies between isolates differing in host range. Directly adjacent to mtd is a second nonidentical copy of the variable end of mtd called TR (for template repeat), followed by a reverse transcriptase gene. Tropism switching is the result of a TR-dependent reverse transcriptase-mediated process that introduces base pair substitutions leading to amino acid changes at about 20 defined positions in the variable part of mtd. The authors proposed a mechanism for this process analogous to the site-specific retrohoming ability of group II introns.


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