Diversity and Functions of Yeast Communities Associated with Insects

microorganisms Review Diversity and Functions of Yeast Communities Associated with Insects Simon Malassigné, Guillaume Minard, Laurent Vallon, Edwige Martin, Claire Valiente Moro and Patricia Luis * Univ Lyon, Université Claude Bernard Lyon 1, CNRS, INRAE, VetAgro Sup, UMR Ecologie Microbienne, F-69622 Villeurbanne, France; [email protected] (S.M.); [email protected] (G.M.); [email protected] (L.V.); [email protected] (E.M.); [email protected] (C.V.M.) * Correspondence: [email protected] Abstract: Following the concept of the holobiont, insect-microbiota interactions play an important role in insect biology. Many examples of host-associated microorganisms have been reported to drastically influence insect biological processes such as development, physiology, nutrition, survival, immunity, or even vector competence. While a huge number of studies on insect-associated microbiota have focused on bacteria, other microbial partners including fungi have been comparatively neglected. Yeasts, which establish mostly commensal or symbiotic relationships with their host, can dominate the mycobiota of certain insects. This review presents key advances and progress in the research field highlighting the diversity of yeast communities associated with insects, as well as their impact on insect life-history traits, immunity, and behavior. Keywords: insect-microbiota interactions; mycobiota; yeast communities; insects Citation: Malassigné, S.; Minard, G.; Vallon, L.; Martin, E.; Valiente Moro, C.; Luis, P. Diversity and Functions of Yeast Communities Associated with 1. Introduction Insects. Microorganisms 2021, 9, 1552. With nearly one million described species and 5.5 million estimated ones, insects https://doi.org/10.3390/ represent more than 80% of the animal biodiversity on Earth [1]. Such diversity is reflected microorganisms9081552 by a broad spectrum of evolutionary acquired traits, some of them being linked to their feeding mode [2]. The evolutionary success of many insects is closely tied to symbiotic Academic Editor: Jana Seifert associations with microorganisms having complementary potential that is otherwise lack- ing in insects and restricts them when inhabiting an ecologically challenging niche or Received: 30 June 2021 invading new environments [3,4]. Therefore, our understanding of insect biology is facing Accepted: 19 July 2021 a paradigm shift where these higher organisms can no longer be considered as an isolated Published: 21 July 2021 entity and instead should be studied in relation with its microbiota (bacteria, fungi, protists, and viruses) with which it interacts and forms a metaorganism, often referred to as the Publisher’s Note: MDPI stays neutral holobiont [5–8]. with regard to jurisdictional claims in To date, most studies have mainly focused on bacteria which establish parasitic, published maps and institutional affil- commensal, or symbiotic relationships with their hosts by colonizing different tissues iations. such as ovaries [9], cuticle [10], or specialized host cells (bacteriocytes) often grouped into an organ called the bacteriome [11]. However, most of bacterial microbiota inhabit the digestive tract [3,4], which is composed of three regions with specific functions (Figure1). These regions vary extensively in terms of morphology and physicochemical properties Copyright: © 2021 by the authors. across insect orders, factors that are known to greatly influence microbial community Licensee MDPI, Basel, Switzerland. structure [3]. The midgut, which hosts a dense and diverse microbial community in most This article is an open access article insect orders, is the primary site of digestion and absorption [4]. In comparison, few distributed under the terms and studies to date have investigated the bacterial diversity in the foregut (the region dedicated conditions of the Creative Commons Attribution (CC BY) license (https:// to food intake, storage, filtering and partial digestion). In Diptera (including flies and creativecommons.org/licenses/by/ mosquitoes) and Lepidoptera (butterflies and moths), the crop is a ventral diverticulum of 4.0/). the oesophagus that serves as primary storage organ for sugars from the nectar before it Microorganisms 2021, 9, 1552. https://doi.org/10.3390/microorganisms9081552 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, x FOR PEER REVIEW 2 of 19 Microorganisms 2021, 9, 1552 2 of 20 agus that serves as primary storage organ for sugars from the nectar before it is transferred intois transferred the midgut into for the digestion midgut [2]. for digestionInterestingly, [2]. Interestingly,a diverse and a rich diverse bacterial and rich community bacterial wascommunity recently observed was recently in the observed crop of mosqui in the croptoes, ofraising mosquitoes, questions raising about questionssymbiotic aboutasso- ciationssymbiotic occurring associations in this occurring organ [12,13]. in this Finally, organ in [12 the,13 hindgut]. Finally, where in the the hindgut bacterial where density the isbacterial very low density for certain is very insect low fororders certain and insect stronger orders for and others stronger (Figure for 1), others the (Figureabsorption1), the is completedabsorption and is completed feces are formed. and feces are formed. A ovary haemocœl (haemolymph) salivary aorta Malpighian tubules glands heart brain pylorus hindgut ileum rectum pharynx anus crop œsophagus proventriculus vagina midgut foregut ventral nerve cord mouth bacterial density B foregut crop midgut hindgut 5 6 7 8 Figure 1. The internal anatomy of an insect (A) and variability of bacterial density across the Figure 1. The internal anatomy of an insect (A) and variability of bacterial density across the diges- digestive tract (B), taking the bee as example (according to Tofilski A.; http://honeybee.drawwing. tive tract (B), taking the bee as example (according to Tofilski A.; http://honeybee.drawwing.org, accessedorg, accessed on 5 March on 5 March 2021 and 2021 Kešnerová and Kešnerov et al. á[14]).et al. All [14 insects]). All present insects an present internal an cavity internal (the cavity hemocoel)(the hemocoel) containing containing a circulatory a circulatory fluid (hemolymph) fluid (hemolymph) and all and organs all organs forming forming the digestive the digestive (in yel- (in low),yellow), reproductive reproductive (in green), (in green), circulatory circulatory (in red), (in red), respiratory respiratory or nervous or nervous (in (inblue) blue) systems. systems. InsectInsect bacterial bacterial microbiota microbiota offer offer a a wide wide range range of of benefits benefits to to their their host, host, ranging ranging from from increasedincreased fecundity fecundity [15], [15 ],oviposition oviposition [16], [16 and], and longevity longevity [17] [to17 shorter] to shorter larval larval development develop- [18].ment Associated [18]. Associated bacteria bacteria also influence also influence many other many aspects other aspects of insect of biology, insect biology, such as such com- as plementingcomplementing host nutrition host nutrition [19], [facilitating19], facilitating dietary dietary breakdown breakdown [20], [providing20], providing protection protec- againsttion against pathogens pathogens [21,22], [21 ,22and], andperforming performing the thedetoxification detoxification of ofxenobiotics xenobiotics or or dietary dietary componentscomponents [23–26]. [23–26]. The The nature nature of of gut gut microbiota-host microbiota-host associations associations appears appears to to be be variable variable amongamong insects. insects. While While weevils weevils [27] [27, burying], burying beetles beetles [28], [ 28and], andsocial social insects insects such suchas termites as ter- [29,30],mites [ 29bees,30 [31],], bees or [certain31], or certainants [32] ants harbor [32] specialized harbor specialized gut microbial gut microbial communities communities mostly mostly transmitted vertically and representing longstanding microbiota-host interactions, transmitted vertically and representing longstanding microbiota-host interactions, other other insects like fruit flies or mosquitoes are mainly colonized by transient microbial communities acquired from the environment [33,34]. Microorganisms 2021, 9, 1552 3 of 20 While an increasing number of studies on insect-associated microbiota have focused on bacteria, other microbial partners such as fungi have been more neglected [35]. Fungal communities (mycobiota) and more particularly yeasts have been demonstrated to be associated with many insect species [36]. Yeasts, which can dominate the mycobiota of certain insects, establish mostly commensal or symbiotic relationships with their host. Like bacteria, yeasts colonize different tissues, such as cuticle, and some yeast species referred to as yeast-like symbionts (YLS) or endosymbionts are localized in fat body specialized cells (mycetocytes) of certain insect species belonging to the Hemiptera and Coleoptera orders [36]. However, yeasts predominantly colonize the digestive tract where they may act as nutrient providers, digestion facilitators, or protectors against pathogens and toxic compounds [37]. Insects are then highly dependent on their gut microbiota, including yeasts, for their development and survival. Based on the degree of dependence, their association can be classified as obligate (or primary) and facultative (or secondary). If YLS located in the mycetocytes of the planthopper Nilaparvata

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