The Dynamics of Cooperative Bacterial Virulence in the Field

Abstract

<jats:p>Laboratory experiments have shown that the fitness of microorganisms can depend on cooperation between cells. Although this insight has revolutionized our understanding of microbial life, results from artificial microcosms have not been validated in complex natural populations. We investigated the sociality of essential virulence factors (crystal toxins) in the pathogen<jats:italic>Bacillus thuringiensis</jats:italic>using diamondback moth larvae (<jats:italic>Plutella xylostella</jats:italic>) as hosts. We show that toxin production is cooperative, and in a manipulative field experiment, we observed persistent high relatedness and frequency- and density-dependent selection, which favor stable cooperation. Conditions favoring social virulence can therefore persist in the face of natural population processes, and social interactions (rapid cheat invasion) may account for the rarity of natural disease outbreaks caused by<jats:italic>B. thuringiensis.</jats:italic></jats:p>

Division of labour and terminal differentiation in a novel Bacillus thuringiensis strain

“…Here we show that division of labour increases the spore yield of LM1212, at least in relation to a canonical Bt strain that produces Cry toxin in every sporulating cell. Cry toxin production is very costly, and invertebrate hosts represent a fixed pool of resource, so that mixed infection of Cry toxin producers and Cry null mutants can produce more viable spores per host than pure infections of Cry toxin producers (Raymond et al, 2012). Peak spore production of Bt in lepidopteran larvae occurs in infections initiated with between 40% and 80% toxin producers (Raymond et al, 2012).…”

“…In Bt, the cost of the production of Cry toxin inclusions is Division of labour in B. thuringiensis C Deng et al substantial both in terms of pure mass (B25% of the total dry weight of Bt) and metabolism (Agaisse and Lereclus, 1995). Crystal toxins are considered as public goods because they can be exploited by cheaters that do not produce such proteins in the insect host (Agaisse and Lereclus, 1995;Raymond et al, 2012). In LM1212, the crystal producer makes a crystal that fills nearly half of the inflated cell (Figures 1a and b).…”

“…In the LM1212 strain, the crystal producers account for only about 40% of the final population, so we hypothesized that LM1212 would yield more spores than a competing Bt strain that produces crystals in all sporulating cells, as crystal toxin production has substantial metabolic costs (Agaisse and Lereclus, 1995;Raymond et al, 2012). We tested this hypothesis in single-strain spore yield experiments and in competition experiments between LM1212 and HD73.…”

“…However, public goods' cooperation is particularly susceptible to competition from cheaters, non-producing strains that can exploit the products of cooperators but gain a growth advantage by avoiding the costs of production themselves (Griffin et al, 2004;Sandoz et al, 2007;West et al, 2007;Raymond et al, 2012). Although population structuring, or high relatedness, may reduce competition with Cry toxin cheaters (Raymond et al, 2012), this social conflict is likely to be a substantial selective force. Indeed, genetically diverse Cry toxin null strains in the B. cereus group can compete with toxin producers in a range of invertebrate hosts (Raymond et al, 2007;Kho et al, 2011).…”

“…In Bt, the critical public good is solubilized Cry toxin in the insect midgut (Raymond et al, 2012). However, public goods' cooperation is particularly susceptible to competition from cheaters, non-producing strains that can exploit the products of cooperators but gain a growth advantage by avoiding the costs of production themselves (Griffin et al, 2004;Sandoz et al, 2007;West et al, 2007;Raymond et al, 2012).…”