Ecology of Microbial Invasions: Amplification Allows Virus Carriers to Invade More Rapidly When Rare

Abstract

Locally adapted residents present a formidable barrier to invasion . One solution for invaders is to kill residents . Here, we explore the comparative ecological dynamics of two distinct microbial mechanisms of killing competitors, via the release of chemicals (e.g., bacteriocins ) and via the release of parasites (e.g., temperate phage ). We compared the short-term population dynamics of susceptible E. coli K12 and isogenic carriers of phage varphi80 in experimental cultures to that anticipated by mathematical models using independently derived experimental parameters. Whereas phages are a direct burden to their carriers because of probabilistic host lysis, by killing competitor bacteria they can indirectly benefit bacterial kin made immune by carrying isogenic phage. This is similar to previously described bacteriocin-mediated effects. However, unlike chemical killing, viable phage trigger an epidemic among susceptible competitors, which become factories producing more phage. Amplification makes phage carriers able to invade well-mixed susceptibles even faster when rare, whereas chemical killers can only win in a well-mixed environment when sufficiently abundant. We demonstrate that for plausible parameters, the release of chemical toxins is superior as a resident strategy to repel invasions, whereas the release of temperate phage is superior as a strategy of invasion.

Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

“…While this is clearly bad news for the individual bacterium (now dead), low rates of phage lysis have been shown to increase the competitiveness of the surviving bacterial population. [47,[55][56][57] Infectious phage particles are released into the environment, where they infect and kill susceptible bacteria in a self-sustaining wave of infection. Because temperate phages usually provide their host cells with super-infection immunity, [58] bacteria that are lysogenized by the same temperate phage -most likely to be the clone mates of the now deceased individual cell -are immune to infection.…”

“…Temperate phage-mediated competition allows lysogens to invade from rare, because of the amplifying nature of viral infection where each subsequent infection yields yet more infectious phages. [55] Consequently, this process is likely to enhance the fitness of colonizing bacteria, facilitating invasion of a resident community. Consistent with this, lysogens have been shown to invade a population of non-lysogens of P. aeruginosa in rat lungs.…”

What traits are carried on mobile genetic elements, and why?

“…As well as having an effect on the bacterial host, many horizontally transferred genes also code for traits that can affect the fitness of a host's neighbours. This can be either in a positive way, by producing proteins that can have a beneficial effect on the degrading enzymes of the host's neighbours (Livermore, 1995), or in a negative way, by producing substances that harm the host's neighbours, such as bacteriocins (Dykes and Hastings, 1999;Riley and Wertz, 2002;van der Ploeg, 2005;Brown et al, 2006).…”

The unavoidable costs and unexpected benefits of parasitism: Population and metapopulation models of parasite-mediated competition

“…While few explicit models of this idea exist (Brown et al, 2006;Tompkins et al, 2003), one can trace the genesis of the idea to early work on apparent competition. In the first model of apparent competition in a host-microparasite system, Holt and Pickering (1985) found that in the presence of a parasite that infects two distinct populations, the population with relatively low resistance would be displaced by the more resistant population.…”

“…For example, it is thought that parasite-mediated apparent competition played a role in the ecological displacement of native red squirrels by grey squirrels in England (Tompkins et al, 2003). Additionally, competition experiments conducted in laboratory demonstrated that a temperate phage could facilitate the invasion of its bacterial host in new environments occupied by other bacteria (Brown et al, 2006). The ubiquity of parasites in nature and their potential for affecting ecological interactions warrants a close look into the mechanisms determining the outcome of parasite-mediated competition.…”