Hacquard, S.

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Disentangling the factors shaping microbiota composition across the plant holobiont

CommentaryDisentangling the factors shapingmicrobiota composition acrossthe plant holobiontIntroductionHealthy and asymptomatic plants in nature are colonized by a richdiversity of microbes comprising bacteria, fungi, protists and viruses(i.e. the plant microbiota), forming complexmicrobial consortia thatimpact plant growth and productivity. Consequently, plants mustnot be viewed as autonomous entities but rather as holobionts (amacrobe and its numerous microbial associates), within which allinteracting organisms contribute to the overall stability of the system(Vandenkoornhuyse et al., 2015). More than a century ago, Hiltnerhypothesized that the resistance of plants towards pathogenesis isdependent on the composition of plant microflora and that rootexudates of different plants could support development of differentmicrobial communities (Hartmann et al., 2008). The developmentof next generation sequencing technologies and associatedcomputational analytical tools now allows the detailed investigationof these important concepts (Bulgarelli et al., 2012; Lundberg et al.,2012). However, despite the fact that the plant microbiota researchfield shows exponential growth (Fig. 1),most of the studies publishedso far have focused on one particular microbial kingdom and/orspecific host niches. There is consequently a need for a more holisticunderstanding of the microbial communities associated with differ-ent plant compartments and discerning which factors shape thesemicrobial assemblages across the plant holobiont. In this issue ofNewPhytologist, Coleman-Derr et al. (pp. 798–811) provide a compre-hensive analysis of the structure of both fungal and bacterialcommunities in the rhizosphere, phyllosphere, leaf and rootendosphere, as well as proximal and distal soil samples fromcultivated and native agaves. Since agaves spp. are adapted tonutrient-poor environments, extreme drought and elevated temper-atures, these plants represent important models for the plantmicrobiota research field because they are likely to host an importantreservoir of beneficial microbes that may support their survival.Structural convergence of the bacterial microbiota ofplantsIt is now well established that root colonization by soil bacteria is adeterministic and tightly controlled process involving differentselective steps. Edaphic factors determine the start inoculum of thesoil biome whereas rhizodeposits and host genotype mediatebacterial community shifts from soil communities to host-adaptedcommunities with reduced diversity (Bulgarelli et al., 2013).Therefore, the roots of phylogenetically unrelated plant speciesassemble overall structurally related bacterial communities belong-ing to only four major bacterial phyla (Proteobacteria, Actinobac-teria, Bacteroidetes and Firmicutes), with Proteobacteria andAcidobacteria community members being consistently enrichedand depleted, respectively, in plant roots compared to theirsurrounding soil biome (Hacquard et al., 2015). Importantly,Coleman-Derr et al. report here that bacterial communities associ-ated with agave plants growing in arid environments also share thistaxonomic signature, indicating that the selective forces shaping rootmicrobiota composition at a high taxonomic rank are robust againsta wide range of host plants and environmental conditions. Incontrast with the bacterial microbiota of plant roots for which thestart inoculumcan be easily defined, it is assumed that leaf-associatedbacterial communities are more subject to stochastic variations dueto the multiple and more complex inoculum sources (Maignienet al., 2014).Consistentwith this,Coleman-Derr et al. show that leafendosphere communities show higher variability across seasons thanthe root endopshere communities. Nonetheless, they could identifycore prokaryotic taxa that are shared between endophytic compart-ments, including microbiota members belonging to Actinobacteria,Bacilli, Alpha-, Beta- and Gamma-proteobacteria that may conferplant fitness benefits during the dry season. Remarkably, despitebeing harvested 2000 km apart in their respective natural habitats,agave-associated bacterial communities were more impacted byplant compartment thanbybiogeography of thehost (Fig. 2a).Theirresults suggest that geographically distant bacterial inputs canconverge into an overall reproducible taxonomic structure in eachagave compartment. It is nevertheless important to note that asubstantial fraction of the bacterial, but also the fungal communities,is shared between compartments, raising the possibility of extensivereciprocal relocation of microbiota members between belowgroundand aboveground plant tissues.‘Remarkably, despite being harvested 2000 km apart intheir respective natural habitats, agave-associated bacterialcommunities were more impacted by plant compartmentthan by biogeography of the host.’Distinct factors shape fungal and bacterialassemblages on plantsEven though less attention has been given to the fungal microbiotaof plants, fungal communities appear to be hyper-diverse in both454 New Phytologist (2016) 209: 454–457  2015 The AuthorNew Phytologist 2015 New Phytologist Trustwww.newphytologist.comForumaboveground and belowground plant tissues, and are dominated bytwo major phyla (Ascomycota and Basidiomycota). However, incontrast with the bacterial microbiota of plant roots, the fungalcommunities seem to be subject to greater variations that are knownto be highly dependant on biogeography, host species and plantcompartment, but which may also include a non-negligiblestochastic component (Shakya et al., 2013). One key aspect inthe experimental design used byColeman-Derr et al.was to analyseagave communities from distant geographical sites to evaluatewhether biogeography of the host similarly impacts fungal andbacterial assemblages. Overall, they found that the major factordriving fungal assemblages in agave plants is the geographic originof the host, contrastingwith bacterial assemblages that are primarilysculpted by plant compartment (Fig. 2a). Their findings indicatethat distinct factors shape fungal and bacterial assemblages onplants and also confirm that fungal and bacterial biogeographymayFig. 1 Exponential increase of the plant microbiota research field. The total number of entries corresponding to the different keywords was evaluated for thetime period 1980–2014 using Google Scholar.(a) (b)Fig. 2 Factors influencing microbial community establishment across the plant holobiont. (a) Percentage of the variance explained by the factors ‘hostbiogeography’, ‘compartment’ and ‘season’ for both bacterial and fungal communities associated with agave plants. The results that are presented wereadapted from Coleman-Derr et al. (this issue of New Phytologist, pp. 798–811). (b) Schematic representation of the plant holobiont (grey), the multispeciesinteractions network within the plant holobiont (orange) and the external factors that may impact its stability (brown). 2015 The AuthorNew Phytologist 2015 New Phytologist TrustNew Phytologist (2016) 209: 454–457www.newphytologist.comNewPhytologist Commentary Forum 455differ fundamentally on large scales. Unlike bacteria, but similar toplants and animals, distribution of fungi might be primarilyconstrained by climate and dispersal limitation, which may favourhigher endemism in fungal compared to bacterial populations(Bonito et al., 2014; Talbot et al., 2014). This is consistent with thepositive correlation observed between plant and fungal richness,suggesting these two kingdoms respond similarly to climatic andedaphic variables (Tedersoo et al., 2014). It is likely that habitat-specific features drive assemblages of distinct plant-associatedfungal communities with high levels of functional redundanciesacross sites (i.e. conferring plant fitness benefits against awide rangeof stresses) but also non-negligible site-specific functional capabil-ities (i.e. conferring plant fitness benefits against local stresses).Cultivation practices and microbial communitydisturbanceSince the colonization of land by ancestral plant lineages 450million years ago, plants and microbes have interacted with eachother (Field et al., 2015). This long co-evolutionary process haslikely shaped plant-associated microbial assemblages and selectedfor beneficial interactions across the plant holobiont. Onefundamental question in plant microbiota research is whethercultivation practices can destabilize indigenous and locally adaptedmicrobial communities and whether disturbance can modifyprevalence of a particular disease (Fig. 2b). In humans, it has beenpostulated that hygiene measures aimed at reducing the microbialload in our environments may have instead favoured modernallergic andmetabolic diseases, likely due to the loss of our ancestralcommensal microbes (Blaser & Falkow, 2009). Although thenumber of sampling sites selected by Coleman-Derr et al. was notsufficient to draw a general principle regarding how cultivationpractices altermicrobial community establishment, they found thatcultivated agave harbour less prokaryotic diversity than native agavein the rhizosphere and phyllosphere compartments. This loss ofprokaryotic diversity was largely explained by the dominance ofsome bacterial genera belonging to the family Enterobacteriaceae,among which some members are well known pathogens of agavecausing ‘soft rot’ disease. The findings of Coleman-Derr et al. areconsistent with the idea that agricultural practices that includecontinuousmonoculture, the utilization of germ-free seedlings andhomogenous genetic plant material may perturb heritability ofnative microbial consortia and favour emergence of latentpathogens (Santhanam et al., 2015).The microbiota of the plant holobiont: what’s next?Although the structure of both fungal and bacterial communities inthe leaves and roots of several plant species has been elucidated,there is still a lack of knowledge regarding how multi-organismalinteractions shape microbiota composition across the plantholobiont (Hacquard & Schadt, 2015). More particularly, itremains unclear how competition and cooperation amongmicrobes or between different microbial kingdoms influencemicrobial community establishment. It is likely that plant-associated microbiota members have evolved sophisticatedstrategies to interact with each other within complex microbialconsortia in order to persist in particular host niches. Understand-ing plants as holobionts therefore implies careful investigation ofthese often neglected microbe–microbe interactions (Fig. 2b).Disentangling the interplay between host, microbial and environ-mental factors is also needed to better understandmicrobiota nichespecialization and adaptation to a specific plant compartment.Large-scale isolation and establishment of reference culturecollections of plant-associated microbiota members is a prerequi-site for addressing these important concepts and represents apromising way for reconstituting complex microbial ecosystemsin vitro with germ-free plants (Lebeis et al., 2015). Thesereductionist approaches using synthetic microbial communitieswill have profound implications for the plant microbiota researchfield, allowing a transition from correlation- to causation-basedstudies.AcknowledgementsThe author would like to thank Francis Martin for giving him theopportunity to write this commentary, Paul Schulze-Lefert for hiscontinuous support and scientific advice as well as William ChanzRobbins, Stijn Spaepen and Paloma Duran for their criticalcomments regarding this commentary. The author would also liketo thank the funding sources: the Max-Planck Society and theEuropean Research Council.Stephane HacquardDepartment of Plant Microbe Interactions, Max Planck Institutefor Plant Breeding Research, 50829 Cologne, Germany(tel +49 221 5062 322; email hacquard@mpipz.mpg.de)ReferencesBlaser MJ, Falkow S. 2009.What are the consequences of the disappearing humanmicrobiota? 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Theimportance of themicrobiomeof the plant holobiont.NewPhytologist206: 1196–1206.Key words: bacterial community, fungal community, microbiome, phyllosphere,plant holobiont, plant–microbe interaction, rhizosphere.www.newphytologist.comwww.newphytologist.comnp-centraloffice@lancaster.ac.uknp-usaoffice@lancaster.ac.uk27 2015 The AuthorNew Phytologist 2015 New Phytologist TrustNew Phytologist (2016) 209: 454–457www.newphytologist.comNewPhytologist Commentary Forum 457

Disentangling the factors shaping microbiota composition across the plant holobiont

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