Phage and bacteria support mutual diversity in a narrowing staircase of coexistence

Abstract

The competitive exclusion principle states that phage diversity M should not exceed bacterial diversity N. By analyzing the steady-state solutions of multistrain equations, we find a new constraint: the diversity N of bacteria living on the same resources is constrained to be M or M þ 1 in terms of the diversity of their phage predators. We quantify how the parameter space of coexistence exponentially decreases with diversity. For diversity to grow, an open or evolving ecosystem needs to climb a narrowing 'diversity staircase' by alternatingly adding new bacteria and phages. The unfolding coevolutionary arms race will typically favor high growth rate, but a phage that infects two bacterial strains differently can occasionally eliminate the fastest growing bacteria. This contextdependent fitness allows abrupt resetting of the 'Red-Queen's race' and constrains the local diversity.

Population Dynamics of Phage and Bacteria in Spatially Structured Habitats Using Phage λ and Escherichia coli

“…Many of the theoretical works on phage-bacterium interactions have assumed well-mixed populations (20)(21)(22)(23)(24). Even though they provide tremendous insights, such assumptions may predict quite unstable population fluctuations, while even in chemostat experiments the population fluctuations are an order of magnitude less than predicted (21).…”

“…Furthermore, phages are found to be major carriers of genes between prokaryotes (12), including pathogens. For example, a number of toxin genes are phage borne: the cholera toxin gene in Vibrio cholerae (13-15), the diphtheria toxin in Corynebacterium diphtheriae (16,17), the gene for toxic shock syndrome toxin 1 in Staphylococcus aureus (18), and Shiga toxins in the enterohemorrhagic strains of Escherichia coli (15,19).Many of the theoretical works on phage-bacterium interactions have assumed well-mixed populations (20)(21)(22)(23)(24). Even though they provide tremendous insights, such assumptions may predict quite unstable population fluctuations, while even in chemostat experiments the population fluctuations are an order of magnitude less than predicted (21).…”

Phage Life Cycles Behind Bacterial Biodiversity

“…More aggressive phages win the competition because of higher burst size, better adhesion rates or shorter latent periods. This competition underscores that the diversity of bacteria is always higher than the diversity of phages, which gives bacteria an edge in the "arms race" [116] Under favorable conditions, the higher growth rate is beneficial for both bacteria and lytic phages [116]. According to "killing the winner" hypothesis, the dominance of susceptible bacteria population in limited niches implies accessibility of high numbers of the host cells for rapid phage propagation.…”

“…Moreover, a superinfection exclusion (Sie) mechanism protects the bacterial host from secondary infection by closely related phages, being another factor driving phage evolution. Differences in phageresistance, induced by temperate phages, lead to higher diversification among virulent lytic phages [116,118,119]. Knowles et al (2016) propose the "piggyback the winner" model in which highly dense populations suffer greater selection pressure to initiate lysogenic cycles, which maintains both high density of bacteria and the phage population.…”

Population cycles and species diversity in dynamic Kill-the-Winner model of microbial ecosystems

“…In the classical Kill-the-Winner (KtW) model of Thingstad 5 virulent phages reduce populations of their susceptible hosts to a low steady state level, which is independent of hosts' growth rate thus allowing multiple species per nutrient type. The number of co-existing bacterial species in the resulting ecosystem is determined exclusively by the parameters of phage predation 5 , the topology of the phage-bacterial infection network [6][7][8] , and the carrying capacity of the environment 4,[7][8][9] . Microbial populations are routinely exposed to more dynamics than assumed in the traditional steady state KtW model and its variants.…”