Biological warfare: Microorganisms as drivers of host–parasite interactionsInfection, Genetics and Evolution

About

Authors
Nolwenn M. Dheilly, Robert Poulin, Frédéric Thomas
Year
2015
DOI
10.1016/j.meegid.2015.05.027
Subject
Microbiology (medical) / Genetics / Ecology, Evolution, Behavior and Systematics / Molecular Biology / Microbiology / Infectious Diseases

Similar

A diffusion model for host–parasite interaction

Authors:
Fabio Augusto Milner, Curtis Allan Patton
2003

Host-Parasite Interactions in Trypanosomiasis: on the Way to an Antidisease Strategy

Authors:
N. Antoine-Moussiaux, P. Buscher, D. Desmecht
2009

Text

12 4 5 6 7 8 c 9 10 bDepartment of Zoology, University of Otago, Dunedin 9016, New Zealand 11 cMIVEGEC (UMR CNRS/IRD/UM1/UM2 5290), 911 Avenu 1213 14 1 6 a r t i c l e i n f o 17 Article history: 18 Received 3 March 2015 19 Received in revised form 26 May 2015 20 Accepted 27 May 2015 21 Available online xxxx 22 23 24 25 26 27 28 29 3 0 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 . . . . . . . . . . . . 00 59 . . . . . . . . . . 60 . . . . . . . . . . 61 . . . . . . . . . . 62 63 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 64 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 65 66 ⇑ Corresponding author.

E-mail address: Nolwenn.dheilly@stonybrook.edu (N.M. Dheilly).

Infection, Genetics and Evolution xxx (2015) xxx–xxx

Contents lists available at ScienceDirect

Infection, Genetics and Evolution

MEEGID 2358 No. of Pages 9, Model 5G 28 May 20155. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 001. Introduction: host and parasite-associated microorganisms are key players in the phenotypic alterations induced by parasites 2. The disruptive strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. The biological weapon strategy. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4. Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .http://dx.doi.org/10.1016/j.meegid.2015.05.027 1567-1348/ 2015 Published by Elsevier B.V.

Please cite this article in press as: Dheilly, N.M., et al. Biological warfare: Microorganisms as drivers of host–parasite interactions. Infect. Gene (2015), http://dx.doi.org/10.1016/j.meegid.2015.05.027. . . 00 . . . 00 . . . 00imate basis of parasite strategies, to predict their evolutionary dynamics and potentially to prevent therapeutic failures.  2015 Published by Elsevier B.V.

ContentsKeywords:

Holobiont

Symbiosis

Parasitism

Microorganisms

Microbiome

Interactione Agropolis, BP 64501, FR-34394 Montpellier Cedex 5, France a b s t r a c t

Understanding parasite strategies for evasion, manipulation or exploitation of hosts is crucial for many fields, from ecology to medical sciences. Generally, research has focused on either the host response to parasitic infection, or the parasite virulence mechanisms. More recently, integrated studies of host– parasite interactions have allowed significant advances in theoretical and applied biology. However, these studies still provide a simplistic view of these as mere two-player interactions. Host and parasite are associated with a myriad of microorganisms that could benefit from the improved fitness of their partner. Illustrations of such complex multi-player interactions have emerged recently from studies performed in various taxa. In this conceptual article, we propose how these associated microorganisms may participate in the phenotypic alterations induced by parasites and hence in host–parasite interactions, from an ecological and evolutionary perspective. Host- and parasite-associated microorganisms may participate in the host–parasite interaction by interacting directly or indirectly with the other partner. As a result, parasites may develop (i) the disruptive strategy in which the parasite alters the host microbiota to its advantage, and (ii) the biological weapon strategy where the parasite-associated microorganism contributes to or modulates the parasite’s virulence. Some phenotypic alterations induced by parasite may also arise from conflicts of interests between the host or parasite and its associated microorganism.

For each situation, we review the literature and propose new directions for future research.

Specifically, investigating the role of host- and parasite-associated microorganisms in host–parasite interactions at the individual, local and regional level will lead to a holistic understanding of how the co-evolution of the different partners influences how the other ones respond, both ecologically and evolutionary. The conceptual framework we propose here is important and relevant to understand the prox-Dheilly Nolwenn M. , Poulin Robert , Thomas Frédéric a School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY 11794-5000, USAa,⇑ bReview

Biological warfare: Microorganisms as drivers of host–parasite interactions journal homepage: www.elsevier .com/locate /meegidt. Evol. 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131indirectly in the host–parasite interaction. For the purpose of this 132article, we focus on the parasite strategies that result from these 133interactions as summarized in Fig. 2. Host- and parasite134associated microorganisms participate in the phenotypic alteration 135resulting from parasitism and hence in the development of strate136gies for evasion, manipulation or exploitation of hosts and their 137defenses. We discuss how the holobiont perspective could resolve 138issues pertaining to the evolution of hosts, parasites and their asso139ciated microorganisms. This theoretical framework is supported by 140empirical data from various model species. We review the litera141ture and propose new directions for future research on the 142neglected role of associated microorganisms. 1432. The disruptive strategy 144Until now, most studies have focused on the role of 145host-associated microorganisms in determining the host pheno146type. They have revealed remarkable examples of traits that were 147originally assumed to be the product of host genes but have since 148been shown to result from the interaction with its associated 149microorganisms, especially in the context of health and disease. 150These include phenotypic traits such as resistance to parasites, 151heat tolerance, diet choice, and development (Clemente et al., 1522012; Feldhaar, 2011; McFall-Ngai et al., 2013). In particular, these 153findings call for a complete re-evaluation of the immune system 154and its evolution (Dheilly, 2014; McFall-Ngai, 2007). The Host 155holo-immunome (Dheilly, 2014) includes the host-encoded 156immune defense systems, whose maturation and efficiency are 157influenced by the microbiota (indirect interaction Fig. 1A (Buffie 158and Pamer, 2013; Chung et al., 2012; Schnupf et al., 2013; Weiss (white circle) or parasite (gray square). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) tics a