title: Parasites and competitors suppress bacterial pathogen synergistically due to evolutionary trade-offs.
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.
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.
authors.forename: Xiaofang
authors.initials: X
authors.lastname: Wang
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.
authors.forename: Zhong
authors.initials: Z
authors.lastname: Wei
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.
authors.forename: Mei
authors.initials: M
authors.lastname: Li
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.
authors.forename: Xueqi
authors.initials: X
authors.lastname: Wang
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.
authors.forename: Anqi
authors.initials: A
authors.lastname: Shan
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.
authors.forename: Xinlan
authors.initials: X
authors.lastname: Mei
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.|Institute for Environmental Biology, Ecology & Biodiversity, Utrecht University, Padualaan 8, 3584CH, Utrecht, the Netherlands.
authors.forename: Alexandre
authors.initials: A
authors.lastname: Jousset
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.
authors.forename: Qirong
authors.initials: Q
authors.lastname: Shen
authors.affiliation: Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, China.
authors.forename: Yangchun
authors.initials: Y
authors.lastname: Xu
authors.affiliation: Department of Biology, University of York, Wentworth Way, York, YO10 5DD, United Kingdom.
authors.forename: Ville-Petri
authors.initials: VP
authors.lastname: Friman
mesh_terms: D000220:Adaptation, Biological; D000898:Antibiosis; D000069977:Bacillus amyloliquefaciens / Q000502:physiology*; D001435:Bacteriophages / Q000502:physiology*; D005075:Biological Evolution; D018551:Solanum lycopersicum / Q000382:microbiology; D043368:Ralstonia solanacearum / Q000502:physiology* / Q000821:virology*; D058441:Rhizosphere
keywords: Experimental evolution; fitness cost; interference competition; phage therapy, Ralstonia solanacearum; trade-off