The evolutionary consequences of plasticity in host-pathogen interactions

Interactions between individuals such as hosts and pathogens are often characterized by substantial phenotypic plasticity. Pathogens sometimes alter their exploitation strategies in response to defensive strategies adopted by their host and vice versa. Nevertheless, most game-theoretic models developed to explain the evolution of pathogen and host characteristics assume that no such plasticity occurs. Allowing for phenotypic plasticity in these models is difficult because one must focus on the evolution of pathogen and host reaction norms, and then allow for the potentially indefinite reciprocal changes in pathogen and host behaviour that occur during an infection as a result of their interacting reaction norms. Here, we begin to address these issues for a simple host-pathogen system in which the pathogen exhibits a level of virulence and the host exhibits a level of immune clearance. We find, quite generally, that plasticity promotes the evolution of higher levels of cooperation, in this case leading to reduced levels of both virulence and clearance.     

The consequences of volatile organic compound mediated bacterial and fungal interactions

Microbial interactions via infochemicals are fundamental to the development of spatial distribution and activity variations in ecosystems. Microorganisms produce a wide range of infochemicals, frequently secondary metabolites, most of which are soluble and many volatile. Volatile organic compounds (VOCs) have been identified in soil atmospheres and related to community structure and function. VOC profiles produced by microorganisms are consistent, relating to cultural conditions, environment and inputs, and so to population and function dynamics. VOC-mediated interactions can result in functional responses by the organisms involved that result in selective advantage to some community members. Positive, negative or neutral interactions can occur between a very wide range of soil bacteria and fungi. These effects include both stimulation and inhibition of growth, by 40 and 60%, respectively, and enzyme production. These effects are usually transient, e.g. removal of an antagonist is followed by complete recovery. Up- and down-regulation of gene expression, by mRNA and protein profiling has been demonstrated. VOCs have played an important role during the evolution of microorganisms in the context of their communities. This revised version was published online in August 2006 with corrections to the Cover Date.     

Cytology of fungal pathogens and plant-host interactions

Imaging plays a unique role in fungal cell biology and phytopathology by allowing for the documentation of molecular structure in individual fixed and living cells. Advances in fluorescence laser techniques, including confocal and multiphoton microscopy, are opening new avenues for cellular exploration. These techniques hold tremendous potential for studies of host-pathogen interactions including the use of genetically encoded markers such as green fluorescent protein, in situ hybridization and fluorescence resonance energy transfer.     

Extracellular enzyme localization during interspecific fungal interactions

Abstract Confronted colonies of Phlebia radiata, P. rufa, Coriolus versicolor, Stereum hirsutum, Phanerochaete velutina and Hypholoma fasciculare showed spatially and temporally heterogeneous patterns of loccase-α-naphthol and peroxidase activities. These activities were coincident in axenic cultures. but were not always so during interaction. Confrontation between species resulted in induction of phenoloxidase activities, even within coenocytic colony regions of Phlebia species which were normally void of such activities in axenic culture. These events resulted in restriction of C. versicolor growth during interaction with P. rufa.     

The complex interactions between host immunity and non-biotrophic fungal pathogens of wheat leaves

Significant progress has been made in elucidating the mechanisms used by plants to recognize pathogens and activate “immune” responses. A “first line” of defense can be triggered through recognition of conserved Pathogen or Microbe Associated Molecular Patterns (PAMPs or MAMPs), resulting in activation of basal (or non-host) plant defenses, referred to as PAMP-triggered immunity (PTI). Disease resistance responses can also subsequently be triggered via gene-for-gene type interactions between pathogen avirulence effector genes and plant disease resistance genes (Avr-R), giving rise to effector triggered immunity (ETI). The majority of the conceptual advances in understanding these systems have been made using model systems, such as Arabidopsis, tobacco, or tomato in combination with biotrophic pathogens that colonize living plant tissues. In contrast, how these disease resistance mechanisms interact with non-biotrophic (hemibiotrophic or necrotrophic) fungal pathogens that thrive on dying host tissue during successful infection, is less clear. Several lines of recent evidence have begun to suggest that these organisms may actually exploit components of plant immunity in order to infect, successfully colonize and reproduce within host tissues. One underlying mechanism for this strategy has been proposed, which has been referred to as effector triggered susceptibility (ETS). This review aims to highlight the complexity of interactions between plant recognition and defense activation towards non-biotrophic pathogens, with particular emphasis on three important fungal diseases of wheat (Triticum aestivum) leaves.     

Arbuscular mycorrhizal fungal phylogeny-related interactions with a non-host

Arbuscular mycorrhizal fungi (AMF) form symbiotic relationships with most vascular plants including some gymnosperm species. Although species in the gymnosperm family Pinaceae normally develop ectomycorrhizal associations, AMF hyphae and vesicles, typical of members of the Suborder Glomineae, have been reported in the roots of some Pinaceae species. However, it is not known whether AMF belonging to various species and suborders are able to colonize roots of Pinaceae species and to what extent this influences the performance of Pinaceae seedlings. We tested in each of the Glomaceae, Acaulosporaceae and Gigasporineae AMF families two species for their ability to colonize and affect the growth of Pinus strobus (eastern white pine) in the presence or absence of an AMF host plant (Trifolium pretense—red clover). Glomus intraradices was the only AMF that colonized pine roots, predominantly in the presence of clover, forming intracellular hyphae and vesicles but not arbuscules. Colonization, however, did not relate to increased pine biomass and the overall presence of AMF, regardless of colonization abilities, resulted in a biomass reduction. This effect on pine seedling biomass was explained by the AMF family to which the AMF belonged, indicating that the effects of AMF on the non-host pine may be related to phylogeny. Acaulosporaceae species reduced pine biomass the most whereas, Gigasporineae species had the smallest effect on biomass. These preliminary results suggest that AMF may affect the soil microflora differently among AMF families in previously unsuspected ways with potential consequences for non-AMF host growth.     

Volatile and non-volatile fungal oxylipins in fungus-invertebrate interactions

Eight-carbon volatiles are characteristic of the odour profile of many filamentous fungi. They derive from enzymatic or non-enzymatic lipid oxidation and are thus termed volatile oxylipins. Collectively, non-volatile and volatile fungal oxylipins are important hormone-like factors that regulate the phenotypic status of a fungus, i.e. growth, morphological differentiation and secondary metabolite production. Given this intimate link between oxylipin formation and phenotypic change, we propose that the release of volatile oxylipins is an important means by which fungi may influence the course and outcome of interactions with animals. Such invertebrate – fungus interactions are intricate inter–kingdom relationships where either one depends on the other, or both on each other, where one is to the others benefit or detriment – eventually having even consequences on third parties and thus influencing whole foodwebs. In this review, we first highlight the connections between oxylipin formation and fungal phenotypic changes, how they affect invertebrate interactions and vice versa. We then expand this by implementing eight-carbon volatiles as infochemicals. Infochemicals are cues or signals perceived by the invertebrates' chemical senses, that are to the invertebrates' or the fungus’ benefit or detriment, through the behavioural responses they elicit. We point out, with various examples, that there is a strong analogy between fungus-invertebrate interactions mediated by fungal eight-carbon volatiles and plant-herbivore interactions mediated by six-carbon green-leaf volatiles released from wounded or stressed plants.     

Host-microbe interactions: innate pattern recognition of fungal pathogens

The recognition of fungi is mediated by germline pattern recognition receptors (PRRs) such as Toll-like receptors and lectin receptors that interact with conserved structures of the microorganisms, the pathogen-associated molecular patterns (PAMPs). Subsequently, PRRs activate intracellular signals that collaborate for the efficient activation of the host defense. The specificity of these responses is achieved through the activation of a particular mosaic of PRRs, that is determined by the available fungal PAMPs and the innate immune cells involved. This will determine a divergence of the final type of reaction, and in this way the innate host defense has the capability to deliver tailored responses to each pathogen.     

Evidence of species interactions within an ectomycorrhizal fungal community

Ectomycorrhizal fungal communities can be structured by abiotic and biotic factors. Here, we present evidence for community structuring by species interactions. We sampled ectomycorrhizas and forest floor seven times during a 13-month period. The presence of various ectomycorrhizal fungal species was determined for each sample, and species co-occurrence analyses were performed. For both ectomycorrhizas and forest floor samples there was significantly less co-occurrence among species within the community than expected by chance, mostly because of negative associations involving Cenococcum geophilum or Clavulina cinerea. For some species pairs, there was significantly more co-occurrence than expected by chance. Both nitrogen and tannin additions to the forest floor altered some interactions among species. The causes of these nonrandom distributions are currently unknown. Future investigations on competition, antibiosis, parasitism and facilitation among ectomycorrhizal fungal species appear to be warranted.     

Amblypygid-fungal interactions: The whip spider exoskeleton as a substrate for fungal growth

Fungi and arthropods represent some of the most diverse organisms on our planet, yet the ecological relationships between them remain largely unknown. In animals, fungal growth on body surfaces is often hazardous and is known to cause mortality. In contrast, here we report the presence of an apparently non-harmful mycobiome on the cuticle of whip spiders (Arachnida: Amblypygi). The associations are not species-specific and involve a diversity of fungal species, including cosmopolitan and local decomposers as well as entomopathogens. We discuss the ecology of the detected fungal species and hypothesize that the thick epicuticular secretion coat of whip spiders (the cerotegument) promotes fungal growth. It is possible that this relationship is beneficial towards the host if it leads to parasite control or chemical camouflage. Our findings, which are the first from this arthropod lineage, indicate that non-pathogenic interactions between arthropods and fungi may be much more widespread than predicted and call for more studies in this area.     

Semaphorin-neuropilin-1 interactions in plasticity and regeneration of adult neurons

During development, axonal growth cones are guided to their appropriate targets by many attractive and repulsive cues. It has become increasingly clear over the last few years that how the growth cone responds to these cues depends both on the molecular nature of the cue and on the internal state of the neuron. The unexpected result is that the same molecule can act as an attractor or as a repellent. A number of guidance cues used by neurons during development are retained in the adult nervous system, where their function is often still unclear. Most of these molecules are implicated in plasticity in the adult nervous system and can play a role (sometimes maladaptive) in neuronal regeneration after injury. A group of axonal guidance cues that has been well studied in development is the semaphorin family of secreted and membrane-anchored proteins, which has been implicated in axon steering, fasciculation, branching and synapse formation. This review focuses on semaphorin-3A (probably the best-characterized semaphorin) and its receptors (in particular neuropilin-1) in the adult nervous system and argues that semaphorin-3A plays a role in the maintenance and regeneration of adult sensory neurons.     

Local cortical interactions determine the form of cortical plasticity.

Competitive interactions between left and right eye inputs to visual cortex during development are usually explained by the thalamocortical axons competing more or less well for cortical territory during retraction into eye specific domains. Here we review the evidence for competitive and co-operative interactions between cortical columns in barrel cortex which are present several weeks after retraction of thalamocortical axons into barrels. Sensory responses in barrel cortex can be altered by a period of vibrissa deprivation. It was found that responses to previously deprived vibrissae (that had been allowed to regrow) were depressed more if neighboring vibrissae were spared than if all vibrissae were removed simultaneously. Depression of the deprived vibrissa response was greater the closer the cell lay to a spared barrel. It was also found that spared vibrissae responses were potentiated more if several neighboring vibrissae were left intact than if only a single vibrissae was spared. These results suggest a mechanism of cooperative potentiation, perhaps due to intracortical summation of excitation evoked by neighbouring vibrissa stimulation. Thalamic responses to vibrissa stimulation were unaffected by deprivation indicating a cortical origin. One of the consequences of deprivation was that the speed of transmission between barrels was increased for spared and decreased for deprived vibrissa. These results imply that inherent interactions between cortical columns give rise to a property of competition and co-operativity which amplify the effects of sensory deprivation.     

Contamination by uranium mine drainages affects fungal growth and interactions between fungal species and strains

The presence of aquatic hyphomycetes has been reported for several heavy metal-contaminated waters. Tolerance probably is one adaptation to coping with heavy metals. To help clarify this issue strains of two species of aquatic hyphomycetes (Tricladium splendens Ingold and Varicosporium elodeae Kegel) were isolated from a reference stream and a stream contaminated with heavy metals and grown on malt extract agar prepared with reference and contaminated water to characterize colony morphology, growth rate, growth inhibition and interaction among species and strains. In V. elodeae the morphology of colonies differed between strains. Colony diameter increased linearly over time with growth rates being lower for strains isolated from contaminated than from reference streams (mostly for V. elodeae). Strains from the contaminated stream grew faster in medium prepared with contaminated water than in medium prepared with reference water, while for strains from the reference stream there was no significant difference in growth rates on the two media. In interacting isolates radial growth toward the opposing colony was generally lower than toward the dish edge. Percentage growth inhibition was higher for isolates in intraspecific interactions (13-37%) than in interspecific interactions (3-27%). However differences in growth inhibition experienced by interacting isolates were observed only in three cases out of 16. The difference between the percentage inhibition caused and experienced by a given isolate was highest in interactions involving isolates with distinct growth rates. Our results suggest that strains from the reference stream tolerate heavy metals while strains from the contaminated stream seem to be adapted to contaminated waters. We hypothesize that in natural environments fungal species-specific limits of tolerance to metal contamination might determine an abrupt or gradual response of the original fungal community to mine pollution giving origin to a poorer fungal community dominated by adapted strains with distinct functional efficiency.     

Spatially segregated SNARE protein interactions in living fungal cells

The machinery for trafficking proteins through the secretory pathway is well conserved in eukaryotes, from fungi to mammals. We describe the isolation of the snc1, sso1, and sso2 genes encoding exocytic SNARE proteins from the filamentous fungus Trichoderma reesei. The localization and interactions of the T. reesei SNARE proteins were studied with advanced fluorescence imaging methods. The SSOI and SNCI proteins co-localized in sterol-independent clusters on the plasma membrane in subapical but not apical hyphal regions. The vesicle SNARE SNCI also localized to the apical vesicle cluster within the Spitzenk?rper of the growing hyphal tips. Using fluorescence lifetime imaging microscopy and Foerster resonance energy transfer analysis, we quantified the interactions between these proteins with high spatial resolution in living cells. Our data showed that the site of ternary SNARE complex formation between SNCI and SSOI or SSOII, respectively, is spatially segregated. SNARE complex formation could be detected between SNCI and SSOI in subapical hyphal compartments along the plasma membrane, but surprisingly, not in growing hyphal tips, previously thought to be the main site of exocytosis. In contrast, SNCI.SSOII complexes were found exclusively in growing apical hyphal compartments. These findings demonstrate spatially distinct sites of plasma membrane SNARE complex formation in fungi and the existence of multiple exocytic SNAREs, which are functionally and spatially segregated. This is the first demonstration of spatially regulated SNARE interactions within the same membrane.     

Host-microbe interactions: fungi invasive human fungal opportunistic infections

Jean-Paul's research interest is focused on the analysis of the structure and biosynthesis of the cell wall of Aspergillus fumigatus and its interaction with the host. The A. fumigatus genome will now be used to understand multifactorial systems such as fungal virulence of an opportunistic fungus in an immunocompromised host and assembly and regulation of cell wall polymer rearrangement under the control of the environment.     

Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions

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