Parasites and competitors suppress bacterial pathogen synergistically due to evolutionary trade-offs.

Xiaofang Wang,Anqi Shan,Alexandre Jousset,Qirong Shen,Ville-Petri Friman,Mei Li,Yangchun Xu,Zhong Wei,Xinlan Mei,Xueqi Wang

doi:10.1111/evo.13143

Abstract

Parasites and competitors are important for regulating pathogen densities and subsequent disease dynamics. It is, however, unclear to what extent this is driven by ecological and evolutionary processes. Here, we used experimental evolution to study the eco‐evolutionary feedbacks among Ralstonia solanacearum bacterial pathogen, Ralstonia‐specific phage parasite, and Bacillus amyloliquefaciens competitor bacterium in the laboratory and plant rhizosphere. We found that while the phage had a small effect on pathogen densities on its own, it considerably increased the R. solanacearum sensitivity to antibiotics produced by B. amyloliquefaciens. Instead of density effects, this synergy was due to phage‐driven increase in phage resistance that led to trade‐off with the resistance to B. amyloliquefaciens antibiotics. While no evidence was found for pathogen resistance evolution to B. amyloliquefaciens antibiotics, the fitness cost of adaptation (reduced growth) was highest when the pathogen had evolved in the presence of both parasite and competitor. Qualitatively similar patterns were found between laboratory and greenhouse experiments even though the evolution of phage resistance was considerably attenuated in the tomato rhizosphere. These results suggest that evolutionary trade‐offs can impose strong constraints on disease dynamics and that combining phages and antibiotic‐producing bacteria could be an efficient way to control agricultural pathogens.

Highlights

Microbial species interactions can affect disease dynamics by changing the relative and absolute pathogen densities in the hostassociated microbiomes (Mendes et al 2011; Mueller and Sachs 2015; Wei et al 2015b; Donaldson et al 2016)
Phage and B. amyloliquefaciens decreased pathogen densities most efficiently in combination indicative of a synergistic effect (Fig. 1A, D; Table 1a, d). One explanation for this could be that both phages and B. amyloliquefaciens had higher population densities when cultured together leading to more efficient pathogen density reduction
We found that B. amyloliquefaciens exerted stronger antagonism toward the pathogen compared to the phage

Summary

Introduction

Microbial species interactions can affect disease dynamics by changing the relative and absolute pathogen densities in the hostassociated microbiomes (Mendes et al 2011; Mueller and Sachs 2015; Wei et al 2015b; Donaldson et al 2016). Evolving resistance does not come for free and often leads to fitness costs in terms of poorer functioning of some other bacterial life-history trait Such evolutionary trade-offs include, for example, reduced bacterial growth (Hall et al 2012; Scanlan et al 2015) via loss of phage receptors that are used by the phage and by the bacteria to uptake nutrients (Lenski and Levin 1985), reduced bacterial ability to adapt to abiotic conditions (Scanlan et al 2015), impairment of mismatch-repair genes (Pal et al 2007), and reduced expression of bacterial virulence genes (Addy et al 2012a). It is still somewhat unclear if antibiotic selection makes pathogens more susceptible to phages

Methods

Results

Conclusion