Phenomena that are directly associated with phage secondary infection or adsorption of already phage-infection bacteria include the above-noted lysis from without plus mechanisms of resistance to lysis from without (Abedon, 1994; Abedon, 1999). Both phenomena possibly play roles in the life history of certain phages, most notably the T-even phages, allowing for resistance to the premature lysis of cultures as mediated by secondary adsorption (i.e., resistance to lysis from without) along with a means of eventually assuring the lysis of those cultures, i.e., so-called lysis-inhibition collapse (Abedon, 1992; Abedon, 1999; Abedon, 2009a). Secondary infection is also seen in the parasitism of phage infections by satellite phages, such as phage P4's parasitism of phage P2 infections. See Turner and Duffy (2008) for discussion of the evolutionary ecology of phage-on-phage parasitism and Hyman and Abedon (2012) for its consideration in viral systems more generally. In addition, there is the also above-noted superinfection exclusion and superinfection immunity.
These latter two phenomena operate by distinctly, conceptually different mechanisms (Hyman and Abedon, 2010), with superinfection exclusion a blockage as expressed by primary phages especially on the successful phage genome translocation into the adsorbed bacterium (Abedon, 1994) whereas superinfection immunity is a post genome-translocation mechanism by which subsequent secondary phage genetic contribution to infections is curtailed, though not always successfully (Fogg, et al., 2010). From the terms employed, we can view these phenomena literally as prevention (or exclusion) of secondarily adsorbing phages from superinfecting (superinfection exclusion) versus resistance (i.e., immunity) of a primary infection to the continuation of infection by secondary phages that nonetheless have successfully initiated superinfection (superinfection immunity).
Note that Berngruber et al. (2010) collectively describe these two otherwise mechanistically distinct phenomena of blockage on successful secondary infection as superinfection inhibition. To the extent that secondary infection gives rise to some degree of coinfection then we can also consider what have been described as mutual exclusion, partial exclusion, or the depressor effect. These respectively are the prevention of replication of one of two lytically coinfecting but not closely related phages, essentially mutually exclusion but between closely related phages, and reductions in burst sizes given coinfection between phages that are not clonally related (Abedon, 1994). That is, to the extent that they act against phages that are secondarily infecting, then these mechanisms might be viewed as ones of partial or incomplete superinfection inhibition.
In practical terms, the consequence of a failure of secondary infection is loss of the secondarily adsorbing phage. This loss occurs because the secondary phage must commit to adsorbing–that is, irreversible adsorption–prior to testing the infection status of the now adsorbed bacterium. The result inevitably is an ecological loss of phages, one which can be considered to be a potential mechanism of virion inactivation that is in addition to nucleic acid or virion-protein damage. This loss of secondary phages is of issue when phages are being employed as antibacterial agents, e.g., (Abedon et al., 2011), since phages display one-hit killing kinetics of bacteria (Bull and Regoes, 2006) and thus any more than one adsorbing phage to a single bacterium represents a loss of antibacterial agent. This loss of secondary phages as killing agents occurs regardless of whether superinfection inhibition is expressed by the primary infection since a single bacterial cell at most can only support a single phage burst. In addition, partial interference between coinfecting phages–i.e., mutual exclusion, partial exclusion, or depressor effect– can result in reductions of the productivity of resulting infections that in turn could result, for example, in less effective in situ phage amplification in numbers and/or poor phage penetration into bacterial biofilms (Abedon and Thomas-Abedon, 2010).
Table 1. Distinguishing among secondary infection varieties
We would expect partial interference between coinfecting phages to occur particularly given phage therapy treatments that employ cocktails of otherwise not full coinfection-compatible phage strains. Resulting reductions in infection productivity during phage therapy, however, may be less of a concern given the formulation of infection-incompatible phages into cocktails (Chan et al., 2013; Chan and Abedon, 2012) so long as coinfection does not occur until late in phage population growth (i.e., until after most or all bacteria have already been bactericidally adsorbed), if passive rather than active treatments are employed (see below), or instead if phages are applied in multiple doses to infections rather than in just a single application (e.g., see arguments for multiple versus single dosing made in Abedon, 2012a; Abedon, 2014).
From a non-applied perspective the superinfecting phage, even if otherwise "wasted" in terms of bacterial killing, nevertheless may still survive to some degree genetically. This survival may be measured in terms of the proportion of a burst that is associated with the secondary phage's genome (Abedon, 1994), though it remains an open question whether the associated proportional loss of primary phage genetic contribution to such bursts in fact evolutionarily selects for mechanisms of superinfection inhibition (Abedon, 1999). Of far greater relevance, however, is the contribution of secondary phage genetic survival to phage genome evolution, that is, as can result phage genomic mosaicism (Hatfull and Hendrix, 2011; Hendrix et al., 1999; Hendri et al., 2008). Whether the associated recombination between phages is a consequence of coinfection during lytic infections, the superinfection of lysogenic infections, or in some manner occurring between prophages, unless two phages have initially adsorbed simultaneously then coinfections are a consequence of secondary infections, and particularly parallel secondary infections.