Available online at www.sciencedirect.com

ScienceDirect Microbe–microbe interactions determine oomycete and fungal host colonization Eric Kemen Microbial organisms sharing habitats aim for maximum fitness that they can only reach by collaboration. Developing stable networks within communities are crucial and can be achieved by exchanging common goods and genes that benefit the community. Only recently was it shown that horizontal gene transfer is not only common between prokaryotes but also into eukaryotic organisms such as fungi and oomycetes benefiting communal stability. Eukaryotic plant symbionts and pathogens coevolve with the plant microbiome and can acquire the ability to communicate or even collaborate, facilitating communal host colonization. Understanding communal infection will lead to a mechanistic understanding in how new hosts can be colonized under natural conditions and how we can counteract. Addresses Max Planck Institute for Plant Breeding Research, Carl-von-Linne´ Weg 10, Cologne 50829, Germany Corresponding author: Kemen, Eric ([email protected], [email protected])

Current Opinion in Plant Biology 2014, 20:75–81 This review comes from a themed issue on Biotic interactions 2014 Edited by Makoto Hayashi and Martin Parniske

http://dx.doi.org/10.1016/j.pbi.2014.04.005 1369-5266/Published by Elsevier Ltd.

Introduction Microbial colonization of almost all aquatic and terrestrial habitats would not have happened without microbes collaborating. Long term coevolution and cooperation such as endosymbiosis, leading to organelles like mitochondria and chloroplasts, have been studied extensively. We are only now getting evidence of two or more species that can coevolve quickly, change evolutionary directions several times and interact with various partners [1]. Such ‘short term’ cooperation leads to geographic mosaics of adaptation and massive microbial diversity [2]. Interactions between microbes, however, can take different forms such as parasitism, mutualism or commensalism. Categorizing these interactions is difficult and one should rather think of a continuum, as microbe-derived effects are often context-dependent and influenced by www.sciencedirect.com

abiotic or biotic factors [3], in particular the position of an organism in a network of different food chains. While great progress has been made in recent years studying parasitic and mutualistic host–microbe interactions on a mechanistic level, most research used reductionist approaches focusing on interactions between only the two organisms. Studies on the human microbiome [4] or the plant leaf and root microbiome [5] suggest a complex host system with multipartite interactions. Recent findings revealed not only hosts being associated with microbes, but parasites and symbionts themselves carrying microbes that are potentially beneficial or harmful for one or both sides [6,7]. The aim of this paper is to highlight microbe–microbe interactions in mutualistic and pathogenic plant symbiosis in the light of complex microbiota and social behavior. I propose that host–microbe specificity under natural conditions is not only determined by both organisms interacting directly, but by their microbiota cooperating or opposing each other.

Microbe–microbe interactions Microbes in general evolve to reach maximum reproductive success under given environmental conditions [8]. Therefore, they only engage in or maintain a costly cooperation in case this increases their fitness to a level comparable or above free-living organisms that do not interact or do not have a benefit from interaction [9]. For example cross feeding is an important mechanism in microbe–microbe interactions to stabilize cooperation. Combining two Escherichia coli mutants that are unable to produce certain amino acids but complement each other by overproducing the corresponding amino acid revealed an even higher fitness when grown together compared to E. coli wildtype alone [10]. This example of a synthetic community study reveals that loosing genes of costly pathways can increase fitness if collaboration partners contribute missing metabolites to a pool of common goods. Under natural conditions complex networks to share goods have evolved that partially resemble economical markets [11]. For example microbial members of such a market have to be careful of choosing a trading partner from which they benefit and that does not cheat or exploit them. When Foster et al. [12] co-cultivated different microbial species that had been isolated from a common aquatic environment in synthetic communities of two and more isolates, they observed in the majority of interactions net negative fitness. From these Current Opinion in Plant Biology 2014, 20:75–81

76 Biotic interactions 2014

results one can conclude that a majority of random interactions is competitive rather than cooperative [12]. Following the idea of microbial market strategies as proposed by Werner et al. [11], microbes have to build local ties, diversify or specialize, become indispensible, build storage and eliminate competitors to not be cheated and to be successful in microbial communities. Examples for such tight, highly specialized communities are mainly from anaerobic degradation processes: due to low or even negative energy yield during degradation of numerous substrates under anaerobic conditions, microbes require collaborators that remove unwanted metabolic products to shift the reaction equilibrium towards the desired direction and therefore increase fitness or in case of endothermal reactions enable survival at all [13]. Under aerobic conditions common goods are frequently generated by secretion of enzymes needed for substrate degradation. Fungi, such as white-rot causing species secrete a broad range of such enzymes with hydrolytic activity to degrade lignocellulose-rich material, resulting in the release of sugars and phenolic compounds [14]. Such products are attractive substrates for a broad range of bacteria leading to diverse bacterial associations [15]. Studies have shown that a coexisting bacterium even promotes the growth of a white-rot fungus [16], however mechanisms are unknown. The question however remains what are all the other associated bacteria doing and is the fungus just a bad trader being exploited by cheaters? Phylogenetically diverse microbial communities such as bacterial-fungal communities are in general less stable to cheaters than communities of closely related microbes [17]. This is due to cooperators antagonizing phylogenetically related cheaters more efficiently, since excluding a distantly related cheater with broad range sensors, such as sensors for detecting free sugars, is more difficult than excluding highly specific close relatives [17]. Another important point is that a cheater under one condition can be a beneficial collaborator under another condition. Strains of Pseudomonas aeroginosa that lack quorum sensing and iron-scavenging siderophore production are cheaters under conditions where both traits are needed but are not, if no siderophores are needed or quorum sensing is irrelevant as has been shown in several experiments [18]. For the example with a white-rot fungus this could mean that bacteria are cheaters as long as they only metabolize sugars needed by the fungus, but once toxic side products such as phenols and organic acids accumulate that can be metabolized by associated bacteria but inhibit the fungus [14], they become beneficial collaborators and fitness for all members of the community has increased. In summary, the evolutionary outcome of a cooperating microbial community that has increased fitness by producing common goods is an assortment of individuals with Current Opinion in Plant Biology 2014, 20:75–81

similar and/or complementary interests [9]. This leads to formation of new species and species complexes that depend on each other to survive.

Horizontal gene transfer increases speed of communal adaptation Expression of the Nlb gene for autonomous replication of Tobacco etch virus (TEV) in tobacco plants, revealed, that a wild type TEV passed through this plants for several generation lost its Nlb gene from its genome [19]. The resulting virus showed increased fitness compared to wild type but lost the ability to grow on wilt type Tobacco plants [19]. Similar gene losses of essential enzymes such as cell wall degrading enzymes and pathways such as thiamine biosynthesis present in their host plants have been identified in plant parasitic microbes, in particular obligate biotroph pathogens [20,21] and obligate symbionts such as the arbuscular mycorrhizal fungus Rhizophagus irregularis [22]. Horizontal gene transfer (HGT) might be a tool to reduce genome size in one of the partners and therefore increase fitness depending on biotic and abiotic factors of one or both. Rare HGTs have been described from fungi to plants [23], parasitic flowering plant to host flowering plant [24], bacteria to insect [25] and bacteria to host plants, such as T-DNA transfer by Agrobacterium rhizogenes [26]. More frequent however are exchanges of genetic material by HGT in bacteria–bacteria interactions [27], fungal–fungal or fungal–bacterial interactions in biofilms [21,28]. HGT might be mediated by viruses as vectors of gene transfer into bacterial hosts while bacteria, during host colonization or adaptation as endosymbionts, transfer genes into their eukaryotic host genome [29]. Such endosymbionts in fungi are common, for example prokaryotes in Rhizopus [30] or the microbiome in mycorrhiza fungi [6]. It remains to be elucidated how intracellular organisms contribute to the evolution of their host genome and how transferred genes contribute to social selection and fitness. For osmotrophs like oomycetes and fungi there is certainly a strong evolutionary pressure to acquire depolymerizing enzymes, transporter proteins and metabolic pathways to enable them not only to spread to new environments and utilize new food sources but further to make use and to contribute to common goods in microbial communities [28] that in turn enables these microbes to get rid of energy intensive pathways and therefore increase their own fitness. Polz et al. [31] hypothesize a niche-specific horizontal gene pool mediating the evolution of local networks and niche-specific subpopulations that are stable and adaptive to a continuous organismic exchange in mixed-species biofilms. Such populations, due to a massive local gene-exchange and strong niche-specific selection pressure, can build stable functional networks and interspecies network redundancy that increases the robustness of communities to perturbation. Stable networks in turn strengthen www.sciencedirect.com

Communal host colonization Kemen 77

microbe–microbe dependencies and lead to biofilm formation. Experiments using synthetic mixed-species communities of selected human pathogenic bacteria that are able to form mixed biofilms have revealed enhanced stress resistance such as resistance to antimicrobial compounds, compared to single-species biofilms of the individual members [32]. These findings and experiments highlight the importance to understand mixed biofilm development and progression since mixed biofilms can acquire new properties that might be relevant for host colonization and in particular colonization of new hosts.

Communal virulence Although fungi and other filamentous eukaryotes belong to the so-called rare microbiome in terms of cell numbers compared to prokaryotes, they can have significant impact on host health [33]. Prominent examples in human pathology are yeasts of the genus Candida, with most species being ubiquitous opportunistic pathogens. Under natural conditions, C. albicans induces mixed-species biofilms consisting of bacteria and other fungal species [34]. Pseudomonas aeruginosa, a Gram-negative bacterium is often co-isolated with Candida albicans [35]. Both exhibit extensive signal exchange through secreted signaling molecules and depending on host conditions and available resources, P. aeruginosa suppresses C. albicans growth or promotes its growth and enhances virulence [35]. C. albicans acquired the ability to detect many different bacterial molecules such as peptidoglycans, lipopolysaccharides, proteolytic host products and many more yet unknown signaling molecules that enable the fungus to interact and benefit from living within a heterogeneous microbial community [35]. Like human fungal pathogens, plant-colonizing fungi and oomycetes have evolved to form complex cooperative networks and mixed-species biofilms with host microbiota (Figure 1). Endophytic fungi and bacteria isolated and re-mixed in vitro, revealed that only those competent in stable biofilm formation were able to produce indoleacetic acid like substances, a common good and suppressor of competing microbes [36]. For mutualistic mycorrhiza fungi close interactions with numerous beneficial bacteria, called helper bacteria, have been observed that for example enhance growth and increase fungal branching [37–39]. In a Laccaria bicolor–Pseudomonas fluorescens interaction trehalose and thiamine, respectively, are common goods stabilizing this interaction [40]. Trehalose most likely attracts the bacterium as a carbon-source, while the fungus relies on thiamine provided by the bacterium. Further, the P. fluorescens bacterial type III secretion system that is able to transfer bacterial proteins into host cells has been shown to be essential to promote fungal host colonization [41], revealing not only the importance of metabolites for communal interactions but potentially www.sciencedirect.com

effector proteins as well that might be relevant to manipulate the host. The same P. fluorescens isolate, however, is able to suppress root infection by the pathogenic fungus Gaeumannomyces graminis [42,43]. Context dependency of P. fluorescens response to different fungi highlights the sensitivity by which microbes are able to detect and react to other microbes. We are only just starting to understand how pathogens rely on associated microbes to promote virulence. For example, species of the genus Rhizopus that are pathogenic to plants and humans harbor bacterial endosymbionts of the genus Burkholderia, producing toxins that are essential for fungal virulence [30,44]. The oomycete Phytophthora parasitica releases zoospores from individual zoosporangia that form biofilms on the leaf surface. These ‘intra-species’ biofilms are crucial for successful penetration of the host plant [45]. So far we do not know if under natural conditions such biofilms become mixed-species biofilms. Since inoculum levels under natural conditions are low and signals mediating biofilm formation would be diluted rapidly, Phytophthora species have evolved not only the ability to communicate on a species level, but even with other genera, such as Pythium [46]. Oomycetes, comparable to fungi, have evolved the ability for inter-kingdom communication. By secretion of quorum-sensing mimics, Phytophthora can interfere with bacterial communication [47] and bacteria can induce Phytophthora zoosporangia production [48], highlighting intense signal exchange both ways. It becomes more and more evident that under natural conditions fungal and oomycete species are generally associated with a broad range of bacteria. How specific these interactions are remains to be elucidated. Isolating 29 different bacteria, each from more than 400 fungal leaf endophytes representing different fungal taxa and locations, revealed no taxonomic structure [49]. So where do fungal and oomycete associated bacteria come from? Are host resident bacteria recruited [50]? Prokaryotic patterns in the rhizosphere are conserved across related species and only vary with geographical sites [51] while phyllospheric prokaryotes from natural sites vary from plant to plant even sharing the same geographical site [52]. A reason for this might be strong fluctuation in abiotic perturbation of aerial plant parts versus roots in natural environments. Under greenhouse conditions, phyllosphere communities are reproducible and stable to biotic perturbation [53]. In the rhizosphere a eukaryotic colonizer is therefore more likely to encounter reproducible conditions in the wild, while a phyllosphere-colonizing organism has to be prepared for varying conditions. Adaptive phenotypic plasticity evolves in response to such fluctuating environments and results in high fitness under variable conditions [54]. An example of plasticity in Phytophthora is the production of autoinducer-2 [47], an extracellular signaling molecule that mediates quorum-sensing in diverse bacterial species [55] and might therefore enable the pathogen to recruit Current Opinion in Plant Biology 2014, 20:75–81

78 Biotic interactions 2014

Figure 1

(a) pathogen / mutualist microbiome eukaryotic microbes

viruses

host microbiome eukaryotic microbes

host

pathogen / symbiont

viruses

prokaryotic microbes pathogen / mutualist community members

prokaryotic microbes host community members

(b)

intra-microbiome interactions inter-microbiome interactions

‘classical’ hostmicrobe interaction

(c) Sp

B

B B

Sp

Current Opinion in Plant Biology

Proposed network for an interaction between host microbiota and eukaryotic pathogen/symbiont microbiota. (a) Host colonization by symbionts or parasites can be seen as a gradual interconnection between two networks: one by a pathogen or symbiont and its microbiota and one by the host microbiota. A colonizing organism and its microbiome has to render the host surface and the host microbiome susceptible, a stage that is sensitive to manipulation by cooperating beneficial or detrimental organisms. Bacteria reaching the host surface, along with or attached to the fungal or oomycete spore load, can grow prior to spore germination and interact with the host microbiota and with the host. Likewise, spores might interact with the host microbiome prior to or during germination. Eukaryotic microbes such as grazers on bacteria (e.g. ciliates) might influence early stages of infection by changing bacterial community composition. These early steps are critical for establishing the close host contact that will be required for host manipulation by a symbiont or pathogen. (b and c) Leaf surface with attached oomycete spores (Sp) (from Albugo laibachii) and bacterial colonies (B) growing close to spores prior to spore maturation and germination (pictures have been taken from formaldehyde fixed samples stained with SYTOX Green).

bacteria from different phyla but with redundant function. Functional robustness without the need for structural robustness might be the key for a successful pathogen under natural conditions and might enable colonization of more distant hosts by inducing mixedspecies biofilms including host adapted microbes. This does not exclude, however, a potential need for structural robustness of pathogen-associated communities that travel with pathogens and coevolve over longer terms such as endosymbionts.

Colonization of new hosts as a consequence of communal virulence? Infections of novel hosts by host range expansion or host jumps are the most frequent causes of emerging fungal diseases [56,57]. While importance of such events for genome evolution [58] and increased virulence [59] Current Opinion in Plant Biology 2014, 20:75–81

becomes more and more apparent there is hardly any knowledge of the trigger or mechanism. Several mechanisms have been proposed [60]; however, one point that remains poorly investigated is the microbial context and the ability to acquire new properties in mixed species communities and biofilms. As outlined by Schulze-Lefert and Panstruga [60], asexual clonal propagation during rapid expansion of pathogen populations likely promotes host jumps, given that single founder events may be sufficient for new host colonization. Bacteria might be recruited by eukaryotic colonizers as helpers for such early steps: first, due to their broad host range and distribution; second, their high reproduction rate that enables fast biofilm formation; and third, the ability of some to suppress host immunity (Figures 1 and 2). In particular necrotroph pathogens might benefit from collaborating with hemibiotroph pathogens, such as Pseudomonas syringae [61], since triggering biotroph www.sciencedirect.com

Communal host colonization Kemen 79

Figure 2 (b)

(c)

(d)

(e)

(f)

(g)

(h)

lum low ho ino st m cu an icro lum + tib ios biota i s hig ho h ino st m cu an icro lum tib + ios biot low is a ho ino st cu sy micr lum mb ob + ios iota is hig h ho ino st cu sy micr lum mb ob + ios iota low is in pa ocu l t sy hog um + mb en i hig ont hi n pa ocu sy thog lum mb en + ion t

cu no hi hig

low

ino

cu

lum

fitness costs / individuum

probability of pathogen emergence / infection

(a)

= negative/inhibitory interaction ↔ = positive/promoting interaction = plant microbes

= pathogen-associated microbes Current Opinion in Plant Biology

Expected effects of microbe–microbe interactions on pathogen fitness during early stages of infection. (a) Low inoculum on axenic hosts hampers microbe–microbe interactions and results in maximum effort for each individual pathogen to colonize its host. If host susceptibility is low, fitness costs will be high since infection rates are low and therefore mortality is high. (b) High inoculum levels enable interaction between host colonizing organisms where early successful colonization can support later colonizers, sharing fitness costs and therefore increasing success rates. (c and d) In case a host is colonized by antagonistic organisms, fitness costs increase massively for low inoculum (c) with decreasing costs for sufficiently high inoculum levels (d). In contrast, if host microbes cooperate with the colonizing microbe, fitness costs are significantly reduced for low (e) and high (f) inoculum levels. Absolute gain of fitness, however, depends on costs for establishing and maintaining this collaboration. (g and h) A significant decrease in fitness cost might be expected if a pathogen or a symbiont colonizes a host while being associated with adapted microbes that share costs for making a host susceptible and conditions favorable for colonization.

response and therefore increasing salicylic acid -levels leads to reduced jasmonic acid -levels and therefore reduced necrotroph response. For herbivore insects and their diverse symbiotic bacteria this mechanism has been shown crucial to promote virulence [62]. It has been hypothesized that trade-offs in performance on different hosts promote the evolution of host specificity by blocking host shifts. Although this hypothesis might be true for highly specialized pathogens close to genetic equilibrium, most pathogens are able to colonize multiple related hosts without fitness loss [63,64]. Theses generalists, due to their broad host range, are more likely to interact with a broad range of other organisms compared to specialists [64]. Since phenotypic plasticity can mitigate costs for generalism [64], one might speculate that generalists, to increase plasticity, locally recruit adapted host microbes that nevertheless exhibit functional redundancy, rather than maintaining their own microbes as do obligate biotrophic mycorrhiza fungi that likely have a high dependency on a specific microbe. Microbe–microbe interactions might therefore be www.sciencedirect.com

a major determinant of host range, lifestyle and host specialization under natural conditions.

Conclusion Minimizing fitness costs by collaborating with other organisms is a major evolutionary trait that acts through a combination of optimized reproductive success and survival. Survival of a community strongly depends on its members’ ability to optimize collaboration. Exchange and accumulation of genes benefiting the community are therefore driven by social selection and render populations stable to perturbation. Plant mutualists and pathogens have coevolved with their host microbiome and have acquired the ability to cooperate resulting in microbe– microbe interactions that benefit their host for example in case of enhanced growth and branching of mycorrhiza fungi associated with certain fungi or harm their host in case of microbe–microbe interactions that lead for example to higher penetration efficiencies and increased stress tolerance following biofilm formation. Symbiotic Current Opinion in Plant Biology 2014, 20:75–81

80 Biotic interactions 2014

mutualists, such as mycorrhiza fungi, cooperate with bacteria and significantly lower their own fitness costs by buffering biotic and abiotic perturbations that might lead to sub-optimal conditions (Figure 2). For pathogens we are only just beginning to understand the importance of collaboration and this knowledge might be crucial to our understanding of how new pathogens emerge and how epidemics kick off possibly through interaction with other species (Figure 1). Biocontrol using living microbes has shown that infections can be reduced or stopped but targeted knowledge-based approaches are still rare. A deep understanding of how pathogens interact with environmental microbes will enable us to predict where epidemics might occur and will facilitate targeted approaches to interfere.

Acknowledgements I am grateful to A Kemen, M Agler and J Ruhe for discussions and commenting on the manuscript. I acknowledge funding by the Max Planck Society.

References and recommended reading Papers of particular interest, published within the period of review, have been highlighted as:  of special interest  of special interest 1.

Thompson JN: The dynamics of microbial coevolution. Microbe 2012, 7:349-352.

2.

Laine AL: Role of coevolution in generating biological diversity: spatially divergent selection trajectories. J Exp Bot 2009, 60:2957-2970.

3. 

Hussa EA, Goodrich-Blair H: It takes a village: ecological and fitness impacts of multipartite mutualism. Annu Rev Microbiol 2013, 67:161-178. This article focuses on multipartite symbiosis, in particular mutualism. It highlights the concept of multilayered interactions and findings that show mutualistic benefit as a sum of host–microbe and microbe–microbe interactions. It further discusses how multiple organisms adapt to communal symbiosis.

4.

Eloe-Fadrosh EA, Rasko DA: The human microbiome: from symbiosis to pathogenesis. Annu Rev Med 2013, 64:145-163.

5.

Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P: Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 2013, 64:807-838.

6. 

Desiro A, Salvioli A, Ngonkeu EL, Mondo SJ, Epis S, Faccio A, Kaech A, Pawlowska TE, Bonfante P: Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi. ISME J 2014, 8:257-270. This research article shows, for the first time, that fungi can harbor multiple intracellular bacteria that coexist and cohabit a single cell. As a system, the authors have used an arbuscular mycorrhiza fungus and its naturally occurring endosymbionts.

7.

Scherlach K, Graupner K, Hertweck C: Molecular bacteria–fungi interactions: effects on environment, food, and medicine. Annu Rev Microbiol 2013, 67:375-397.

8.

de Vos MG, Poelwijk FJ, Tans SJ: Optimality in evolution: new insights from synthetic biology. Curr Opin Biotechnol 2013, 24:797-802.

9.

Damore JA, Gore J: Understanding microbial cooperation. J Theor Biol 2012, 299:31-41.

10. Pande S, Merker H, Bohl K, Reichelt M, Schuster S, de Figueiredo LF, Kaleta C, Kost C: Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria. ISME J 2013. Current Opinion in Plant Biology 2014, 20:75–81

11. Werner GD, Strassmann JE, Ivens AB, Engelmoer DJ,  Verbruggen E, Queller DC, Noe R, Johnson NC, Hammerstein P, Kiers ET: Evolution of microbial markets. Proc Natl Acad Sci U S A 2014, 111:1237-1244. This perspectives article gives an important example how cross-disciplinary approaches help to understand complex mechanisms in biology. The authors apply economical theories to microbial community interactions and give examples how this helps to structure our view and future experiments in this field. 12. Foster KR, Bell T: Competition, not cooperation, dominates interactions among culturable microbial species. Curr Biol 2012, 22:1845-1850. 13. Morris BE, Henneberger R, Huber H, Moissl-Eichinger C: Microbial syntrophy: interaction for the common good. FEMS Microbiol Rev 2013, 37:384-406. 14. Boer de W, Folman LB, Summerbell RC, Boddy L: Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 2005, 29:795-811. 15. Herve V, Le Roux X, Uroz S, Gelhaye E, Frey-Klett P: Diversity and structure of bacterial communities associated with Phanerochaete chrysosporium during wood decay. Environ Microbiol 2013. 16. Kamei I, Yoshida T, Enami D, Meguro S: Coexisting Curtobacterium bacterium promotes growth of white-rot fungus Stereum sp. Curr Microbiol 2012, 64:173-178. 17. Jousset A, Eisenhauer N, Materne E, Scheu S: Evolutionary  history predicts the stability of cooperation in microbial communities. Nat Commun 2013, 4:2573. This research article reveals fundamental mechanisms of communal stability. The authors show that phylogenetically diverse communities are rapidly invaded by spontaneous signal-blind mutants, while cooperation is stable in closely related ones. This finding highlights how kin-dependent inhibition links phylogenetic diversity and evolutionary dynamics. 18. Ghoul M, West SA, Diggle SP, Griffin AS: An experimental test of whether cheating is context dependent. J Evol Biol 2014. 19. Tromas N, Zwart MP, Forment J, Elena SF: Shrinkage of genome size in a plant RNA virus upon transfer of an essential viral gene into the host genome. Genome Biol Evol 2014, 6:538-550. 20. Kemen E, Gardiner A, Schultz-Larsen T, Kemen AC, Balmuth AL, Robert-Seilaniantz A, Bailey K, Holub EB, Studholme DJ, MacLean D et al.: Gene gain and loss during evolution of obligate parasitism in the white rust pathogen of Arabidopsis thaliana. PLoS Biol 2011, 9:1-21. 21. Kemen E, Jones JD: Obligate biotroph parasitism: can we link genomes to lifestyles? Trends Plant Sci 2012, 17:448-457. 22. Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V et al.: Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 2013, 110:20117-20122. 23. Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ: Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell 2009, 21:1897-1911. 24. Mower JP, Stefanovic S, Young GJ, Palmer JD: Plant genetics: gene transfer from parasitic to host plants. Nature 2004, 432:165-166. 25. Husnik F, Nikoh N, Koga R, Ross L, Duncan RP, Fujie M, Tanaka M, Satoh N, Bachtrog D, Wilson AC et al.: Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 2013, 153:1567-1578. 26. Chilton M-D, Tepfer DA, Petit A, David C, Casse-Delbart F, Tempe J: Agrobacterium rhizogenes inserts T-DNA into the genomes of the host plant root cells. Nature 1982, 295:432-434. 27. Mitri S, Foster KR: The genotypic view of social interactions in microbial communities. Annu Rev Genet 2013, 47:247-273. 28. Richards TA, Talbot NJ: Horizontal gene transfer in  osmotrophs: playing with public goods. Nat Rev Microbiol 2013, 11:720-727. www.sciencedirect.com

Communal host colonization Kemen 81

This article proposes horizontal gene transfer as a key part of osmotroph evolution to acquire nutrients and to establish communal interactions. 29. Schoenfeld TW, Murugapiran SK, Dodsworth JA, Floyd S, Lodes M, Mead DA, Hedlund BP: Lateral gene transfer of family A DNA polymerases between thermophilic viruses, aquificae, and apicomplexa. Mol Biol Evol 2013, 30:1653-1664. 30. Partida-Martinez LP, Hertweck C: Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 2005, 437:884-888. 31. Polz MF, Alm EJ, Hanage WP: Horizontal gene transfer and the  evolution of bacterial and archaeal population structure. Trends Genet 2013, 29:170-175. This article introduces a model to explain the massive horizontal gene transfer observed in prokaryotic populations. An important factor as highlighted by this article is the need for adaptation to an environmental niche. Niche populations are stabilized by a local horizontal gene pool. The model describes that incoming organisms have to acquire genes from the gene pool to acquire the ability to survive but also contribute new genes that can be utilized by the community. 32. Lee KW, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA: Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J 2014, 8:894-907. 33. Huffnagle GB, Noverr MC: The emerging world of the fungal microbiome. Trends Microbiol 2013, 21:334-341.

45. Galiana E, Fourre S, Engler G: Phytophthora parasitica biofilm formation: installation and organization of microcolonies on the surface of a host plant. Environ Microbiol 2008, 10:2164-2171. 46. Kong P, Tyler BM, Richardson PA, Lee BW, Zhou ZS, Hong C:  Zoospore interspecific signaling promotes plant infection by Phytophthora. BMC Microbiol 2010, 10:313. This research article highlights a dose-dependent success of infection and the ability of different Phytophthora species to communicate and interact with each other above species level. 47. Kong P, Lee BW, Zhou ZS, Hong C: Zoosporic plant pathogens produce bacterial autoinducer-2 that affects Vibrio harveyi quorum sensing. FEMS Microbiol Lett 2009, 303:55-60. 48. Chee KH, Newhook FJ: Relationship of micro-organisms to sporulation of Phytophthora cinnamomi Rands. New Zeal J Agr Res 1966, 9 32-&. 49. Hoffman MT, Arnold AE: Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 2010, 76:4063-4075. 50. Venturi V, da Silva DP: Incoming pathogens team up with  harmless ‘resident’ bacteria. Trends Microbiol 2012, 20:160-164. This paper raises important questions on how local host microbes react to incoming organisms. It concludes by highlighting that host organisms can influence the outcome of diseases.

34. Kolenbrander PE, Palmer RJ Jr, Periasamy S, Jakubovics NS: Oral multispecies biofilm development and the key role of cell– cell distance. Nat Rev Microbiol 2010, 8:471-480.

51. Schlaeppi K, Dombrowski N, Oter RG, Ver Loren van Themaat E, Schulze-Lefert P: Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proc Natl Acad Sci U S A 2014, 111:585-592.

35. Mallick EM, Bennett RJ: Sensing of the microbial neighborhood by Candida albicans. PLoS Pathog 2013, 9:e1003661.

52. Vorholt JA: Microbial life in the phyllosphere. Nat Rev Microbiol 2012, 10:828-840.

36. Bandara WMMS, Seneviratne G, Kulasooriya SA: Interactions among endophytic bacteria and fungi: effects and potentials. J Biosciences 2006, 31:645-650.

53. Maignien L, Deforce EA, Chafee ME, Eren AM, Simmons SL:  Ecological succession and stochastic variation in the assembly of Arabidopsis thaliana phyllosphere communities. mBio 2014:5. This research paper reveals ecological succession and stochastic variation in phyllosphere colonization under controlled conditions. It shows that defined microbial communities are reproducibly built on leaves and that these communities are stable to perturbation by airborne microbes.

37. Bonfante P, Anca IA: Plants, mycorrhizal fungi, and bacteria: a network of interactions. Annu Rev Microbiol 2009, 63:363-383. 38. Deveau A, Palin B, Delaruelle C, Peter M, Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, Frey-Klett P: The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol 2007, 175:743-755. 39. Aspray TJ, Jones EE, Davies MW, Shipman M, Bending GD: Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp. Mycorrhiza 2013, 23:403-410. 40. Deveau A, Brule C, Palin B, Champmartin D, Rubini P, Garbaye J, Sarniguet A, Frey-Klett P: Role of fungal trehalose and bacterial thiamine in the improved survival and growth of the ectomycorrhizal fungus Laccaria bicolor S238N and the helper bacterium Pseudomonas fluorescens BBc6R8. Environ Microbiol Rep 2010, 2:560-568. 41. Cusano AM, Burlinson P, Deveau A, Vion P, Uroz S, Preston GM, Frey-Klett P: Pseudomonas fluorescens BBc6R8 type III secretion mutants no longer promote ectomycorrhizal symbiosis. Environ Microbiol Rep 2011, 3:203-210. 42. Barret M, Frey-Klett P, Boutin M, Guillerm-Erckelboudt AY, Martin F, Guillot L, Sarniguet A: The plant pathogenic fungus Gaeumannomyces graminis var. tritici improves bacterial growth and triggers early gene regulations in the biocontrol strain Pseudomonas fluorescens Pf29Arp. New Phytol 2009, 181:435-447. 43. Chapon A, Guillerm AY, Delalande L, Lebreton L, Sarniguet A: Dominant colonisation of wheat roots by Pseudomonas fluorescens Pf29A and selection of the indigenous microflora in the presence of the take-all fungus. Eur J Plant Pathol 2002, 108:449-459. 44. Partida-Martinez LP, de Looss CF, Ishida K, Ishida M, Roth M, Buder K, Hertweck C: Rhizonin, the first mycotoxin isolated from the zygomycota, is not a fungal metabolite but is produced by bacterial endosymbionts. Appl Environ Microbiol 2007, 73:793-797. www.sciencedirect.com

54. Leggett HC, Benmayor R, Hodgson DJ, Buckling A: Experimental evolution of adaptive phenotypic plasticity in a parasite. Curr Biol 2013, 23:139-142. 55. Neiditch MB, Federle MJ, Miller ST, Bassler BL, Hughson FM: Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2. Mol Cell 2005, 18:507-518. 56. Giraud T, Gladieux P, Gavrilets S: Linking the emergence of fungal plant diseases with ecological speciation. Trends Ecol Evol 2010, 25:387-395. 57. Stukenbrock EH, McDonald BA: The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 2008, 46:75-100. 58. Raffaele S, Kamoun S: Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol 2012, 10:417-430. 59. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ: Emerging fungal threats to animal, plant and ecosystem health. Nature 2012, 484:186-194. 60. Schulze-Lefert P, Panstruga R: A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 2011, 16:117-125. 61. Glazebrook J: Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 2005, 43:205-227. 62. Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW: Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci U S A 2013, 110:15728-15733. 63. Joshi A, Thompson JN: Trade-offs and the evolution of host specialization. Evol Ecol 1995, 9:82-92. 64. Leggett HC, Buckling A, Long GH, Boots M: Generalism and the evolution of parasite virulence. Trends Ecol Evol 2013, 28:592-596. Current Opinion in Plant Biology 2014, 20:75–81

Microbe-microbe interactions determine oomycete and fungal host colonization.

Microbial organisms sharing habitats aim for maximum fitness that they can only reach by collaboration. Developing stable networks within communities ...
964KB Sizes 0 Downloads 4 Views