Herren, Jeremy

Lemaitre, Bruno

Current Opinion in Microbiology

Infoscience - École polytechnique fédérale de Lausanne

Insect–microbe interactions: the good, the bad and the othersEditorial overviewJeremy Herren and Bruno LemaitreCurrent Opinion in Microbiology 2012, 15:217–219For a complete overview see the IssueAvailable online 7th June 20121369-5274/$ – see front matter, # 2012 Elsevier Ltd.All rights reserved.http://dx.doi.org/10.1016/j.mib.2012.05.014Jeremy HerrenGlobal Health Institute, School of LifeScience, EPFL, CH-1015 Lausanne,SwitzerlandJeremy Herren is a PhD student working atthe Global Health Institute (EcolePolytechnique Fe´de´rale de Lausanne,Switzerland) analysing Drosophila-Spiroplasma interactions.Bruno LemaitreGlobal Health Institute, School of LifeScience, EPFL, Station 19, CH-1015Lausanne, Switzerlande-mail: bruno.lemaitre@epfl.chBruno Lemaitre is a Professor working at theGlobal Health Institute (Ecole PolytechniqueFe´de´rale de Lausanne, Switzerland)analysing the basis of microbial infection andthe corresponding host defence responses inDrosophila.The past quarter century has seen a dramatic rise in our understanding of themechanistic basis of insect–microbe interactions. Though not unique inliving in close proximity to microbes, it is not difficult to appreciate thatinsects partly owe their success to being very adept at dealing with them.Studying the response of insects to pathogens has revealed the nature ofreceptors, signalling cascades and effectors that comprise insect immunesystems. Despite not being ‘adaptive’ in the classical immunological sense,insect immunity is clearly multi-faceted, specific and highly effective.Significant progress has also been made on the microbial side with theidentification of a variety of virulence mechanisms that enable microbes toevade, suppress or resist the insect’s immune system. Equally, understand-ing the basis of insect host resistance to microbes has strong implications forlimiting the ability of insects to vector diseases that impact human health ordestroy crops, while facilitating the development of better strategies toprotect beneficial insects, including pollinators.The majority of interactions between insects and microbes are commensal ormutualistic, not pathogenic in nature. It has long been appreciated thatcertain insects incorporate and harness the vast metabolic potential ofmicrobes for their own benefit, such as the mutualistic bacterium Buchnera,which supplies its aphid host with essential amino acids that plant saps lack.Increasingly, we are beginning to appreciate that insect–microbe symbiosesare much more diverse and widespread than was initially thought. Themicrobial flora that colonize insect guts are not only important for theprovision of nutrients, but also have recently been implicated in the abilityof insects to resist infection. Endosymbiotic Wolbachia have long beenstudied for their ability to manipulate the reproduction of their host, buttheir ability to confer their hosts with resistance to viral infection, a featurewhich in large part explains why they are so prevalent, was overlooked untiljust several years ago.In this edition of Current Opinions in Microbiology we have brought together aseries of reviews that cover some aspects of insect–microbe interactions.They not only reveal the recent advances in the field but also reflect thediverse nature of interactions between insects and microbes.It has long been recognized that insects are rather resistant to microbialinfection due to effective physical barriers, including their cuticle or the gutperitrophic matrix as well as a robust, multi-faceted immune response. Asubset of entomopathogenic bacteria such as Bacillus thuringiensis, Serratiaentomophila, Photorhabdus spp. and Xenorhabdus spp. has the capacity tobreach insect barriers either by themselves or (as is the case for Photorhabdusspp. and Xenorhabdus spp.) with the assistance of nematodes, invadingAvailable online at www.sciencedirect.comwww.sciencedirect.com Current Opinion in Microbiology 2012, 15:217–219218 Ecology and industrial microbiologyand proliferating within their host. Initial studies of thesebacteria have mostly focused on their insecticidal toxins,with the goal of developing bio-pesticides. Recent studieshave been revealing the additional layers of complexityinvolved in the infection process. In this issue, Nielsen-Leroux et al. describe the mechanisms used by theentomopathogenic bacteria, B. thuringiensis, Photorhabdusluminiscens and Xenorhabdus spp. to infect insects — frominitial colonization of the gut and hemolymph — toexploitation of the insect cadavers and elimination ofbystanders. An emerging trend is that a diverse rangeof entomopathogens use common strategies to invade andexploit their hosts.Entomopathogenic fungi have the capacity to penetrateinsect cuticles through the production of chitinases andlipases. They are important pathogens of insects in thewild and as such attractive agents for controlling croppests and disease vectors. The study of entomopatho-genic fungi has recently benefited from the developmentof genetic and genomic tools. In their review, Fang et al.examine how, with a comprehensive understanding ofvirulence mechanisms and other aspects of fungalbiology, it has recently become possible to engineer noveland more potent entomopathogenic fungal strains thatcould increase the potential of this method of insectcontrol.Bubonic plague is now widely believed to be the cause ofthe Black Death that swept through Europe in the 14thcentury and killed an estimated 25 million people, repre-senting 30–60% of the European population. Bubonicplague is a zoonotic disease caused by a gram-negativebacterium, Yersinia pestis, circulating mainly among smallrodents and transmitted to humans through fleas. In theirreview, Chouikha and Hinnebusch examine the mechan-istic basis of adaptations that enable Y. pestis to colonizethe flea midgut. Interestingly, Y. pestis had to gain certainfunctions, including biofilm formation and resistance toantibacterial activity, but also lost certain functions,namely insecticidal activity.Phytoplasmas are insect-vectored bacterial plant patho-gens that can have devastating effects on crop yield.Phytoplasma are obligate symbionts of plants (growing inthe phloem) and sap-sucking insects, the latter beingkey for their transmission. Phytoplasmas have a broadplant host range, which often depends on which plantspecies their insect vectors can exploit. Phytoplasmastraverse the gut, pass through the hemolymph and enterthe salivary glands of their hemipteran phloem feedinghosts. Similarly to bacterial endosymbionts, phytoplas-mas have reduced genomes with limited metaboliccapabilities and are not amenable to in vitro culture.Despite these limitations Sugio and Hogenhoutdescribe the considerable advances that has been madein the study of phytoplasma genomic organizationCurrent Opinion in Microbiology 2012, 15:217–219 as well as the identification of specific virulenceeffector proteins produced by phytoplasma to inducechanges in plant physiology. Phytoplasma exemplifyinsect-associated microbes that are highly specializedfor, and almost entirely reliant upon, certain insect hostspecies.Several insect species carry highly integrated bacteriaendosymbionts that provide their host additional meta-bolic capacity allowing survival on an otherwisenutritionally incomplete diet. Examples include theaforementioned Buchnera symbiont of Aphids and Wiggle-sworthia conferring tsetse flies with the ability to useblood meals as their sole food source by providing com-plex B-vitamins. It has long been recognized that endo-symbionts can be lost by rearing insects at highertemperatures. The resulting aposymbiontic insects oftensuffer drastically reduced fitness. In the light of globalwarming models that predict a 1.8–4 8C increase in aver-age temperature, Wernegreen discusses the unexpectedconsequence of climate change on endosymbionticinteractions.Wolbachia infect 40–60% of all insect species, beingamongst the most successful infectious bacteria on earth.As a consequence of their vertical transmission, Wolbachiahave evolved mechanisms to manipulate the reproduc-tion of their hosts. These manipulations include cyto-plasmic incompatibility, which provides Wolbachia with aremarkable capacity to spread through insect populations.Their capacity to spread, in conjunction with the protec-tive effect of Wolbachia against viruses, makes Wolbachia apromising tool for control of disease transmission byinsect vectors. Vavre and Charlat describe recent devel-opments in modelling the spread of Wolbachia throughinsect populations. Predicting the conditions that allowWolbachia to spread through a host population is not onlyof significant biological interest, but also vital for theimplementation of Wolbachia-based disease transmissioncontrol strategies.Fungus-farming ants grow fungi for food by providingfungal gardens with various plant-derived substrates.The symbioses between ants associated microbial biofilmsand cultivated fungi have been largely popularized as astriking example of symbiosis. Specifically, antibiotic-secreting integumental bacteria were believed to haveco-evolved with ants, with a specific role for preventinginfection in fungal gardens. These findings have led toappealing analogies being drawn between ant fungicultureand human agriculture. Here, Mueller reports that after re-examination, the interactions between fungus-farmingants and bacteria appear to be more diverse and do notfit entirely with the picture that was initially presented.While we lack the deep understanding of this field toeither fully accept or refute the conclusions of this review,we felt that when thoughtfully presented and supportedwww.sciencedirect.comEditorial overview Herren and Lemaitre 219by experimental evidence, expression of contradictoryviewpoints is important for scientific advancement.A common condition of the metazoan gut is to be inassociation with a number of benign or beneficial micro-organisms. Recent studies demonstrate that most insectsare associated with a much lower diversity of bacterialtaxa than observed in mammals, and that these areacquired from their environment (food, faeces or egg-shells). Despite their low number, the influence of theseresident microorganisms is profound, altering aspects ofhost physiology, especially digestive and immune func-tions. Here, Ricci et al. examine our understanding notonly of mosquito–microbiota interactions and the implica-tions these have for the general physiology but alsoimmunity of the host insect. Recent advances suggestthat by altering or engineering mosquito microbiota itmight be possible to decrease their competence as humandisease vectors.Mosquitos of the genus Anopheles are the main vectors ofthe human malaria parasite Plasmodium falciparum and as aconsequence are the main target for vector control. WildAnopheles populations are highly heterogeneous in termswww.sciencedirect.com of susceptibility to Plasmodium. Mitri and Vernick describethe progress in understanding the genetic polymorphismsunderpinning mosquito refractoriness to Plasmodium.They reveal how a combination of pre-existing geneticvariation, pathogen-mediated selective pressure and fit-ness trade-offs would have shaped the evolutionaryresponse of vectors to pathogens, leading to vector–pathogen specificity. This review highlights how importantit is to link our understanding of insect immune function toa wider evolutionary and ecological context.These diverse reviews reflect the rapid development ofresearch in the field of insect–microbe interactions, andthe profound impact this work has for human heath andagricultural productivity. Also reflected is a growing needfor a more holistic approach, moving towards more complexmodels involving the simultaneous study of a variety ofmicrobes and environmental conditions. Progress is likelyto be made by studying the interaction between insects andtheir pathogens in the context of non-pathogenic commen-sals and mutualists and vice versa. Researchers are alsoincreasingly appreciating complicated scenarios in whichmicrobes tend to occupy condition-dependent positions onthe spectrum from pathogen to mutualists.Current Opinion in Microbiology 2012, 15:217–219

Insect-microbe interactions: the good, the bad and the others

Jeremy Herren

Bruno Lemaitre

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Insect–microbe interactions: the good, the bad and the others

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Insect-microbe interactions: the good, the bad and the others

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