A cooperative virulence plasmid imposes a high fitness cost under conditions that induce pathogenesis

Abstract

Harbouring a plasmid often imposes a fitness cost on the bacterial host. Motivated by implications for public health, the majority of studies on plasmid cost are focused on elements that impart antibiotic resistance. Plasmids, however, can provide a wide range of ecologically important phenotypes to their bacterial hosts-such as virulence, specialized catabolism and metal resistance. The Agrobacterium tumefaciens tumour-inducing (Ti) plasmid confers both the ability to infect dicotyledonous plants and to catabolize the metabolites that plants produce as a result of being infected. We demonstrate that this virulence and catabolic plasmid imposes a measurable fitness cost on host cells under resource-limiting, but not resource replete, environmental conditions. Additionally, we show that the expression of Ti-plasmidborne pathogenesis genes necessary to initiate cooperative pathogenesis is extremely costly to the host cell. The benefits of agrobacterial pathogenesis stem from the catabolism of public goods produced by infected host plants. Thus, the virulence-plasmid-dependent costs we demonstrate constitute costs of cooperation typically associated with the ability to garner the benefits of cooperation. Interestingly, genotypes that harbour derived opine catabolic plasmids minimize this trade-off, and are thus able to freeload upon the pathogenesis initiated by other individuals.

Agrobacterium tumefaciens recognizes its host environment using ChvE to bind diverse plant sugars as virulence signals

“…Because these mechanisms are usually energy intensive, the controlling system is expected to exhibit very tight regulationactivating virulence pathways under conditions that are not suitable for pathogenic activity would be wasteful (1). However, the pathogen needs to recognize diverse hosts, suggesting that the control system must be very flexible in terms of signal perception.…”

Resource and Competitive Dynamics Shape the Benefits of Public Goods Cooperation in a Plant Pathogen

“…We have experimentally demonstrated that there is a fitness cost associated with harboring the Ti plasmid under resource liming conditions (Platt et al 2011), suggesting that the inequality in Equation 2 is true; however we do not currently know which parameter(s) underlies this cost. Most likely, the cost is a result of differences in mortality rates or utilization efficiencies; however this remains an issue for future work.…”

“…Equilibrial predictions of this model can be graphically represented on a 2-D plot of the resource supply rates (Figure 2). Bearing the Ti plasmid under resourcelimiting conditions imposes significant fitness costs on pTi + cells (Platt et al 2011). Because of this pTi + cells are likely to require a greater minimum supply of non-opine nitrogen sources than pTi − cells.…”

“…pTi + and pTi − cells were competed in AT minimal medium ) supplemented with 0.5% glucose (wt/ vol), 600 μM (NH 4 ) 2 SO 4 , and either 0, 9.4, 37.5, 150, or 600 μM D-octopine. Nitrogen limits the growth of A. tumefaciens strain 15955 when it is grown on 600 μM (NH 4 ) 2 SO 4 (Platt et al 2011), such that under these conditions octopine supplementation provides pTi + cells with an additional, private source of nitrogen.…”

The Agrobacterium Ti Plasmids

“…Indeed, the only Ti plasmid locus required under these conditions is the repABC cassette, which is tightly controlled for maintenance of the Ti plasmid at single copy. Surprisingly, however, there is a significant fitness cost associated with the Ti plasmid under conditions of nutrient limitation, even without induction of the virulence genes (110). Under these conditions, the expression profile of Ti plasmid genes is not expected to vary appreciably from growth in a rich environment, establishing that even the maintenance of this large plasmid at low copy and its vertical transmission during cell division imposes an appreciable metabolic burden.…”