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Coevolution with Bacteriophages Drives Genome-Wide Host Evolution And View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Open Research Exeter 1 Submission Type: Article, Discoveries 2 3 Article Title: Coevolution with bacteriophages drives genome-wide host evolution and 4 constrains the acquisition of abiotic-beneficial mutations 5 1,2,* 1,3 4 1,5 6 Authors Pauline D. Scanlan , Alex R. Hall , Gordon Blackshields , Ville-P. Friman 6 6,7 1,8 7 Michael R. Davis Jr , Joanna B. Goldberg & Angus Buckling . 8 9 Affiliations 1 10 Department of Zoology, South Parks Road, University of Oxford, Oxford OX1 3PS, United 11 Kingdom 2 12 Present Address: Teagasc Food Research Centre, Moorepark, Fermoy, Co Cork, Ireland. 13 Email: [email protected] or [email protected] 3 14 Present Address: Institute of Integrative Biology, ETH Zürich, 8092 Zürich, Switzerland. : 15 Email [email protected] 4 16 Central Pathology Laboratory, Department of Histopathology and Morbid Anatomy, School 17 of Medicine, Trinity College Dublin, Ireland. Email: [email protected] 5 18 Present Address: Imperial College London, Department of Life Sciences, Silwood Park 19 Campus, Buckhurst Road, Ascot Berkshire, SL5 7PY, UK. Email: [email protected] 6 20 Department of Microbiology, Immunology and Cancer Biology, University of Virginia 21 Health System, Charlottesville, Virginia, USA. Email: [email protected] 7 22 Joanna B. Goldberg. Present Address: Department of Paediatrics, Division of Pulmonology, 23 Allergy/Immunology, Cystic Fibrosis and Sleep, Emory University School of Medicine, 24 Rollins Research Center, 510 Clifton Road NE, Suite3009 Atlanta GA 30322, USA. Email: 25 [email protected] 1 8 26 Angus Buckling. Present address: University of Exeter, Penryn Campus, Cornwall, TR10 27 9EZ, UK. Email: [email protected] 28 29 *Corresponding author: Pauline Scanlan, Address: Teagasc Food Research Centre, 30 Moorepark, Fermoy, County Cork, Ireland. Email: [email protected]. 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 2 51 Abstract 52 Studies of antagonistic coevolution between hosts and parasites typically focus on resistance 53 and infectivity traits. However, coevolution could also have genome-wide effects for the host 54 due to pleiotropy, epistasis or selection for evolvability. Here we investigate these effects in 55 the bacterium Pseudomonas fluorescens SBW25 during ~400 generations of evolution in the 56 presence or absence of bacteriophage (coevolution or evolution treatments respectively). 57 Coevolution resulted in variable phage resistance, lower competitive fitness in the absence of 58 phages, and greater genome-wide divergence both from the ancestor and between replicates, 59 in part due to the evolution of increased mutation rates. Hosts from coevolution and evolution 60 treatments had different suites of mutations. A high proportion of mutations observed in 61 coevolved hosts were associated with a known phage target binding site, the 62 Lipopolysaccharide (LPS), and correlated with altered LPS length and phage resistance. 63 Mutations in evolved bacteria were correlated with higher fitness in the absence of phages. 64 However, the benefits of these growth-promoting mutations were completely lost when these 65 bacteria were subsequently coevolved with phages, indicating that they were not beneficial in 66 the presence of resistance mutations (consistent with negative epistasis). Our results show 67 that in addition to affecting genome-wide evolution in loci not obviously linked to parasite 68 resistance, coevolution can also constrain the acquisition of mutations beneficial for growth 69 in the abiotic environment. 70 71 72 73 74 75 3 76 Introduction 77 Parasites are abundant in all natural ecosystems and play a central role in the evolution and 78 ecology of their hosts (Woolhouse et al. 2002). Moreover, antagonistic coevolution (defined 79 as the reciprocal evolution of host resistance and parasite infectivity) is recognised as a key 80 driver of genetic divergence between populations of coevolving hosts and parasites, and by 81 extension, antagonistic coevolution is considered a crucial factor in the origin and 82 maintenance of biodiversity (Buckling and Rainey 2002; Thompson 2005). Host-parasite 83 coevolution between bacteria and their lytic viral parasites, bacteriophages, is studied 84 extensively to understand the cause and consequence of coevolution, as coevolution can be 85 observed over a matter of days and weeks (Bohannan and Lenski 2000). However, in addition 86 to their utility for research, using bacteria and bacteriophage to study coevolution also has 87 important implications for our understanding of the ecology and evolution of microbial 88 populations, the role of phage in the evolution of bacterial virulence and the use of phage in 89 clinical settings (Pirnay et al. 2011; Scanlan and Buckling 2012; Hosseinidoust et al. 2013; 90 Koskella and Brockhurst 2014). 91 92 Coevolution with bacteriophages has many important phenotypic consequences for bacteria, 93 including costs of resistance (Bohannan and Lenski 2000), effects on diversity and niche Alex ! 20/12/14 12:24 94 competition in spatially structured environments (Buckling and Rainey 2002; Brockhurst et Comment [1]: Does this mean reduced growth rate due to phage, or due to resistance? "Reduced population size" or "costs of 95 al. 2004), the social behavior of hosts (Morgan et al. 2012) and evolution of mutation rates resistance" would be better. 96 (Pal et al. 2007). However, little is known about the genomic consequences of bacterial 97 coevolution with phages. While there have been a number of studies using whole genome 98 sequencing (WGS) of coevolved bacteria (Kashiwagi and Yomo 2011; Marston et al. 2012; 99 Le et al. 2014), interpreting the underlying genomic changes is problematic as populations 100 are also adapting to the abiotic environment. An understanding of the genomic consequences 4 101 of coevolution therefore requires a systematic comparison of evolved and coevolved bacterial 102 populations, which is the aim of the current study. Such an experimental approach has been 103 successful in studying the effects of coevolution on virus populations and has revealed that 104 coevolution accelerates molecular evolution in traits linked to infectivity (Paterson et al. 105 2010; Kashiwagi and Yomo 2011), however a similar comparison has yet to be conducted on 106 bacteria. 107 108 Nonetheless, previous theoretical and empirical studies allow us to make general predictions 109 on the potential genomic effects of coevolution with phage. First, we expect greater genomic 110 divergence of hosts among replicates and from the ancestor in coevolving populations. This is 111 because coevolution creates a continually changing selection pressure by generating parasites 112 with novel infectivity alleles and can also select for mechanisms that generate genetic 113 variation i.e. elevated mutation rates and recombination (Hamilton et al. 1990; Pal et al. 114 2007). This prediction is further supported by work on coevolving/evolving viruses and 115 phenotypic studies of bacteria (Buckling and Rainey 2002; Brockhurst et al. 2004). Second, 116 we expect different suites of mutations to be acquired in evolved and coevolved bacteria. 117 Somewhat trivially, we only expect resistance mutations to bacteriophage to be acquired in 118 coevolving populations but a less obvious prediction is that mutations acquired in evolved 119 populations will not be acquired in coevolved populations, despite coevolved hosts 120 experiencing a superset of the selective pressures (i.e. not just abiotic but abiotic plus biotic) 121 experienced by evolved bacteria. This is because coevolution may slow down the acquisition 122 of some beneficial mutations as a result of competition between mutations (clonal 123 interference) (Felsenstein 1974; Gerrish and Lenski 1998) and lower population sizes caused 124 by coevolving parasites (Zhang and Buckling 2011) as well as epistatic interactions between 125 resistance and other mutations (Lenski 1988; Weinreich et al. 2005; Buckling et al. 2006). 5 126 To address these predictions we characterised the genetics of resistance evolution to phage 127 during antagonistic coevolution, detailed the effects of coevolution with phage on genome- 128 wide evolution of bacterial hosts and investigated the relative costs of adaption to the abiotic 129 environment in the presence and absence of coevolving parasites (hereafter referred to as 130 coevolution and evolution treatments). To do so we carried out phenotypic and genomic 131 analyses of the bacterium Pseudomonas fluorescens SBW25 that had been evolved in 132 isolation or coevolved with dsDNA lytic phage (Phi2) for up to 400 generations in nutrient 133 media. These organisms initially undergo an arms race dynamic in these conditions, with 134 bacteria and phage continually evolving resistance and infectivity, while retaining 135 resistance/infectivity to previously encountered populations (Buckling and Rainey 2002). 136 Both increased resistance and infectivity ranges are associated with a growth rate cost relative 137 to ancestral genotypes, and the arms race dynamic can shift to a fluctuating dynamic 138 (temporal changes in the frequency of specialised genotypes) as a result (Hall et al. 2011b). 139 Our initial approach was to focus on the phenotypic and genomic characterization of single 140 genotypes from replicate populations evolved in the presence or absence of phages at
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