Mutualism-parasitism Continuum Research Articles

Phylogeny, morphology, virulence, ecology, and host range of Ordospora pajunii (Ordosporidae), a microsporidian symbiont of Daphnia spp.

The net outcome of symbiosis depends on the costs and benefits to each partner. Those can be context dependent, driving the potential for an interaction to change between parasitism and mutualism. Understanding the baseline fitness impact in an interaction can help us understand those shifts; for an organism that is generally parasitic, it should be easier for it to become a mutualist if its baseline virulence is relatively low. Recently, a microsporidian was found to become beneficial to its Daphnia hosts in certain ecological contexts, but little was known about the symbiont (including its species identity). Here, we identify it as the microsporidium Ordospora pajunii. Despite the parasitic nature of microsporidia, we found O. pajunii to be, at most, mildly virulent; this helps explain why it can shift toward mutualism in certain ecological contexts and helps establish O. pajunii is a valuable model for investigating shifts along the mutualism-parasitism continuum.

Biotic and abiotic controls of nitrogen fixation in cyanobacteria-moss associations.

Most mosses are colonized by nitrogen (N)-fixing cyanobacteria. This discovery is relatively recent, which can explain the large knowledge gaps the field is now tackling. For instance, while we have a good understanding of the abiotic controls (e.g. nutrient availability, increased temperature), we still do not know much about the biotic controls of N2 fixation in mosses. I propose here that we should endeavour to position moss-cyanobacteria associations along the mutualism-parasitism continuum under varying abiotic conditions (e.g. nutrient availability). This would finally unravel the nature of the relationship between the partners and will be a big leap in our understanding of the evolution of plant-bacteria interactions using moss-cyanobacteria associations as a model system.

The Costs and Benefits of Plant-Arbuscular Mycorrhizal Fungal Interactions.

The symbiotic interaction between plants and arbuscular mycorrhizal (AM) fungi is often perceived as beneficial for both partners, though a large ecological literature highlights the context dependency of this interaction. Changes in abiotic variables, such as nutrient availability, can drive the interaction along the mutualism-parasitism continuum with variable outcomes for plant growth and fitness. However, AM fungi can benefit plants in more ways than improved phosphorus nutrition and plant growth. For example, AM fungi can promote abiotic and biotic stress tolerance even when considered parasitic from a nutrient provision perspective. Other than being obligate biotrophs, very little is known about the benefits AM fungi gain from plants. In this review, we utilize both molecular biology and ecological approaches to expand our understanding of the plant-AM fungal interaction across disciplines.

Costs, Benefits, Parasites and Mutualists: The Use and Abuse of the Mutualism–Parasitism Continuum Concept for “Epichloë” Fungi

The species comprising the fungal endophyte genus Epichloë are symbionts of cool season grasses. About half the species in this genus are strictly vertically transmitted, and evolutionary theory suggests that these species must be mutualists. Nevertheless, Faeth and Sullivan (e.g., 2003) have argued that such vertically transmitted endophytes are “usually parasitic,” and Müller and Krauss (2005) have argued that such vertically transmitted endophytes fall along a mutualism-parasitism continuum. These papers (and others) have caused confusion in the field. We used a systematic review to show that close to half of the published papers in this field incorrectly categorize the interaction. Here, we develop the argument that advantages and disadvantages are not the same things as mutualism and parasitism and that experimental evidence must be interpreted in the context of theory. We argue that, contra Faeth and Sullivan, it is highly unlikely that such strictly vertically transmitted endophytes can be parasites, and that, contra Müller and Krauss, it is inappropriate to apply the continuum concept to strictly vertically transmitted endophytes. We develop a mathematical model to support and illustrate our arguments. We use the model to clarify that parasitism requires some degree of horizontal transmission, and that while it is appropriate to use the continuum concept when referring to the genus as a whole, or to species that possess horizontal transmission, we argue that it is inappropriate to use the concept when referring to species that are strictly vertically transmitted.

Context-Dependent Host-Symbiont Interactions: Shifts along the Parasitism-Mutualism Continuum.

AbstractSymbiotic interactions can shift along a mutualism-parasitism continuum. While there are many studies examining dynamics typically considered to be mutualistic that sometimes shift toward parasitism, little is known about conditions underlying shifts from parasitism toward mutualism. In lake populations, we observed that infection by a microsporidian gut symbiont sometimes conferred a reproductive advantage and other times a disadvantage to its Daphnia host. We hypothesized that the microsporidian might benefit its host by reducing infection by more virulent parasites, which attack via the gut. In a laboratory study using field-collected animals, we found that spores of a virulent fungal parasite were much less capable of penetrating the guts of Daphnia harboring the microsporidian gut symbiont. We predicted that this altered gut penetrability could cause differential impacts on host fitness depending on ecological context. Field survey data revealed that microsporidian-infected Daphnia hosts experienced a reproductive advantage when virulent parasites were common while resource scarcity led to a reproductive disadvantage, but only in lakes where virulent parasites were relatively rare. Our findings highlight the importance of considering multiparasite community context and resource availability in host-parasite studies and open the door for future research into conditions driving shifts along parasitism to mutualism gradients.

A Plant-Fungus Bioassay Supports the Classification of Quinoa (Chenopodium quinoa Willd.) as Inconsistently Mycorrhizal.

Quinoa (Chenopodium quinoa Willd.) is becoming an increasingly important food crop. Understanding the microbiome of quinoa and its relationships with soil microorganisms may improve crop yield potential or nutrient use efficiency. Whether quinoa is a host or non-host of a key soil symbiont, arbuscular mycorrhizal fungi (AMF), is suddenly up for debate with recent field studies reporting root colonization and presence of arbuscules. This research seeks to add evidence to the mycorrhizal classification of quinoa as we investigated additional conditions not previously explored in quinoa that may affect root colonization. A greenhouse study used six AMF species, two AMF commercial inoculant products, and a diverse set of 10 quinoa genotypes. Results showed 0 to 3% quinoa root colonization by AMF when grown under greenhouse conditions. Across quinoa genotypes, AMF inoculant affected shoot dry weight (p = 0.066) and height (p = 0.031). Mykos Gold produced greater dry biomass than Claroideoglomus eutunicatum (27% increase), Rhizophagus clarus (26% increase), and within genotype CQ119, the control (21% increase). No treatment increased plant height compared to control, but Funneliformis mosseae increased height compared to C. eutunicatum (25% increase) and Rhizophagus intraradices (25% increase). Although quinoa plants were minimally colonized by AMF, plant growth responses fell along the mutualism-parasitism continuum. Individual AMF treatments increased leaf greenness in quinoa genotypes 49ALC and QQ87, while R. clarus decreased greenness in CQ119 compared to the control. Our research findings support the recommendation to classify quinoa as non-mycorrhizal when no companion plant is present and inconsistently mycorrhizal when conditional colonization occurs.

Conditions Promoting Mycorrhizal Parasitism Are of Minor Importance for Competitive Interactions in Two Differentially Mycotrophic Species.

Interactions of plants with arbuscular mycorrhizal fungi (AMF) may range along a broad continuum from strong mutualism to parasitism, with mycorrhizal benefits received by the plant being determined by climatic and edaphic conditions affecting the balance between carbon costs vs. nutritional benefits. Thus, environmental conditions promoting either parasitism or mutualism can influence the mycorrhizal growth dependency (MGD) of a plant and in consequence may play an important role in plant-plant interactions. In a multifactorial field experiment we aimed at disentangling the effects of environmental and edaphic conditions, namely the availability of light, phosphorus and nitrogen, and the implications for competitive interactions between Hieracium pilosella and Corynephorus canescens for the outcome of the AMF symbiosis. Both species were planted in single, intraspecific and interspecific combinations using a target-neighbor approach with six treatments distributed along a gradient simulating conditions for the interaction between plants and AMF ranking from mutualistic to parasitic. Across all treatments we found mycorrhizal association of H. pilosella being consistently mutualistic, while pronounced parasitism was observed in C. canescens, indicating that environmental and edaphic conditions did not markedly affect the cost:benefit ratio of the mycorrhizal symbiosis in both species. Competitive interactions between both species were strongly affected by AMF, with the impact of AMF on competition being modulated by colonization. Biomass in both species was lowest when grown in interspecific competition, with colonization being increased in the less mycotrophic C. canescens, while decreased in the obligate mycotrophic H. pilosella. Although parasitism-promoting conditions negatively affected MGD in C. canescens, these effects were small as compared to growth decreases related to increased colonization levels in this species. Thus, the lack of plant control over mycorrhizal colonization was identified as a possible key factor for the outcome of competition, while environmental and edaphic conditions affecting the mutualism-parasitism continuum appeared to be of minor importance.

Arbuscular mycorrhizal fungi in changing mountain grassland ecosystems: a challenge for research

Even though arbuscular mycorrhizal fungi (AMF) are present from foothills to all alpine habitats, research on their role in mountain ecosystems remains incomplete. Here we provide a literature review of the ecology and functioning of AMF in mountain ecosystems, as well as their response to global change. We investigated how AM fungal abundance, community composition, and fungal traits are studied under field conditions and are affected by altitude, habitat patchiness, succession, host identity, seasonality, and interaction with other living organisms. The effects of climate change, nutrient enrichment, land-use change, and their interactions are also addressed in this review, as well as the possible applications of AMF for grassland restoration. We show that altitudinal effects on AMF are blurred by other environmental gradients and by host-plant identity. The benefits to plants and possible facilitation effects by AMF in mountain ecosystems have not yet been identified. Based on the stress-gradient hypothesis, the symbiosis between plants and AMF should become more mutualistic with increasing environmental stress. We propose a working hypothesis for the functioning of the AMF–plant interaction along altitudinal gradients by grading it along the mutualism–parasitism continuum, considering current and global climate and environmental change conditions. We conclude by suggesting further research directions.

The rules for symbiont community assembly change along a mutualism-parasitism continuum.

Symbiont community assembly is driven by host-symbiont and symbiont-symbiont interactions. The effects that symbionts exert on their hosts are often context-dependent, and existing theoretical frameworks of symbiont community assembly do not consider the implications of variable outcomes to assembly processes. We hypothesized that symbiont-symbiont interactions become increasingly important along a parasitism/mutualism continuum because; (i) negative outcomes favour host resistance which in turn reduces symbiont colonization and subsequently reduce symbiont-symbiont interactions, whereas (ii) positive host outcomes favour tolerance and consequently higher symbiont colonization rates, leading to stronger interactions among symbionts. We found support for this hypothesis in the cleaning symbiosis between crayfish and ectosymbiotic branchiobdellidan worms. The symbiosis between crayfish and their worms can shift from parasitism/commensalism to mutualism as crayfish age. Here, field surveys identified changes in worm density, diversity and composition that were concomitant to changing symbiosis outcomes. We conducted several laboratory experiments and behavioural assays to relate patterns from the field to their likely causal processes. Young crayfish typically hosted only two relatively small worm species. Older crayfish hosted two additional larger species. In laboratory experiments, young crayfish exhibited a directed grooming response to all worm species, but were unable to remove small species. Conversely, adult crayfish did not exhibit grooming responses to any worm species. Relaxed grooming allowed the colonization of large worm species and initiated symbiont-symbiont intraguild predation that reduced the abundance and altered the behaviour of small worm species. Thus, the dominant processes of symbiont community assembly shifted from host resistance to symbiont-symbiont interactions through host ontogeny and a concomitant transition towards mutualism. This work shows that host resistance can have a prevailing influence over symbiont community assembly when symbiosis is disadvantageous to the host. However, when symbiosis is advantageous and resistance is relaxed, symbiont colonization rate and consequently abundance and diversity increases and interactions among symbionts become increasingly important to symbiont community assembly.

Lotus hosts delimit the mutualism-parasitism continuum of Bradyrhizobium.

Symbioses are modelled as evolutionarily and ecologically variable with fitness outcomes for hosts shifting on a continuum from mutualism to parasitism. In a classic example, rhizobia fix atmospheric nitrogen for legume hosts in exchange for photosynthetic carbon. Rhizobial infection often enhances legume growth, but hosts also incur interaction costs because of root tissues and or metabolites needed to support symbionts in planta. Rhizobia exhibit genetic variation in symbiotic effectiveness, and ecological changes in light or mineral nitrogen availability can also alter the benefits of rhizobial infection for hosts. The net effects of symbiosis thus can range from mutualistic to parasitic in a context-dependent manner. We tested the extent of the mutualism-parasitism continuum in the legume-rhizobium symbiosis and the degree to which host investment can shape its limits. We infected Lotus strigosus with sympatric Bradyrhizobium genotypes that vary in symbiotic effectiveness. Inoculations occurred under different mineral nitrogen and light regimes spanning ecologically relevant ranges. Net growth benefits of Bradyrhizobium infection varied for Lotus and were reduced or eliminated dependent on Bradyrhizobium genotype, mineral nitrogen and light availability. But we did not detect parasitism. Lotus proportionally reduced investment in Bradyrhizobium as net benefit from infection decreased. Lotus control occurred primarily after infection, via fine-scale modulation of nodule growth, as opposed to control over initial nodulation. Our results show how divestment of symbiosis by Lotus can prevent shifts to parasitism.

Different mycorrhizal fungal strains determine plant community response to nitrogen and water availability

AbstractMost research on the mycorrhizal positive–negative responsiveness continuum (or “mutualism–parasitism continuum”) has focused on individual plant species growing at different levels of P availability. Here, we explore this continuum in an experimental plant community inoculated with three arbuscular mycorrhizal (AM) fungal strains (both single and mixed) growing under four resource availability scenarios. These scenarios are a factorial combination of two levels of water and N availability. Each AM fungal strain had a different origin: an arid ecosystem, a farmland, and a mine. We hypothesized that the response of the plant community to mycorrhizal inoculum would depend on the associated AM fungal strain and would be negatively related with increased nitrogen and water availability. Our results showed that mixed‐strain AM fungal inoculation had more positive effects along a wider range of water and N availability scenarios than single‐strain inoculation. In contrast, mycorrhizal growth response of plants inoculated with a single AM fungal strain shifted from positive to neutral and negative depending on resource availability. Adaptation of each strain to its local conditions might confer different properties to the mycorrhizal symbiosis. Therefore, we conclude that AM fungal origin and environmental limiting resources are crucial factors to predict plant community mycorrhizal growth response in changing ecosystems.

The latest news from biological interactions in orchids: in love, head to toe

The latest news from biological interactions in orchids: in love, head to toe

Cleaning mutualist or parasite? Classifying the association between the brittlestar Ophiothrix lineata and the Caribbean reef sponge Callyspongia vaginalis

Symbioses often exist along a mutualism–parasitism continuum, and the classification of any given relationship requires a careful examination of costs and benefits for both symbiont and host. It has been proposed that deposit-feeding by the obligate sponge-dwelling brittlestar Ophiothrix lineata on the surface of the tube sponge Callyspongia vaginalis may increase filtration efficiency resulting in enhanced sponge growth or reproduction while providing protection and food for the brittlestar. However, C. vaginalis produces large (0.5–1.4mm) larvae that are brooded in chambers and released into the interior of sponge tubes year-round, and these larvae could be consumed by O. lineata. In laboratory experiments, brittlestars readily consumed sponge larvae. When larval traps were placed over sponge tubes in the field, fewer larvae per brood chamber were collected from sponge tubes containing brittlestars than sponge tubes that lacked brittlestars, supporting the hypothesis that brittlestars consume sponge larvae under natural conditions. Sponges with brittlestars exhibited no difference in growth or number of brood chambers compared to sponges without brittlestars after 8months, indicating no positive effect of symbiont on host. Spatial and temporal variations in larval release by C. vaginalis likely decrease encounter rates of brittlestars with sponge larvae, reducing the negative impact on the sponge and helping to maintain the association. The available evidence suggests that, depending on the reproductive status of the sponge, the association between O. lineata and C. vaginalis ranges from commensalism to larval parasitism.

How useful is the mutualism-parasitism continuum of arbuscular mycorrhizal functioning?

A recent review in this journal puts forward the premise that our recent studies have resulted in our questioning the validity of the so-called mutualism-parasitism continuum of functioning of arbuscular mycorrhizas. This premise is incorrect and appears largely to result from a misunderstanding of terminology. We clarify a comment in one of our publications that influenced the previous review, which contains several statements that do not accurately represent our views. Our research has overturned not the continuum concept itself, but some past ideas about the balance of resources traded between AM fungi and plants. Of course, we recognize that outcomes of AM symbiosis in relation to the non-mycorrhizal (NM) state are strongly influenced by many environmental factors. Nevertheless, underlying resource trade is always a key determinant of costs and benefits of the symbiosis for both partners. In this context, we address uncertainties and contradictory ideas about mechanisms, causes, effects and outcomes in AM symbioses that occur in the literature, and issues of relevance of research at different scales. We also discuss semantics that can cause confusion. Finally, we assess how useful the mutualism-parasitism continuum is for design of hypothesis-driven experiments to disentangle the complex interactions that determine growth of AM plants, i.e. the so-called emergent properties.

Arbuscular mycorrhizal fungi reduce the differences in competitiveness between dominant and subordinate plant species

In grassland communities, plants can be classified as dominants or subordinates according to their relative abundances, but the factors controlling such distributions remain unclear. Here, we test whether the presence of the arbuscular mycorrhizal (AM) fungus Glomus intraradices affects the competitiveness of two dominant (Taraxacum officinale and Agrostis capillaris) and two subordinate species (Prunella vulgaris and Achillea millefolium). Plants were grown in pots in the presence or absence of the fungus, in monoculture and in mixtures of both species groups with two and four species. In the absence of G. intraradices, dominants were clearly more competitive than subordinates. In inoculated pots, the fungus acted towards the parasitic end of the mutualism-parasitism continuum and had an overall negative effect on the growth of the plant species. However, the negative effects of the AM fungus were more pronounced on dominant species reducing the differences in competitiveness between dominant and subordinate species. The effects of G. intraradices varied with species composition highlighting the importance of plant community to mediate the effects of AM fungi. Dominant species were negatively affected from the AM fungus in mixtures, while subordinates grew identically with and without the fungus. Therefore, our findings predict that the plant dominance hierarchy may flatten out when dominant species are more reduced than subordinate species in an unfavourable AM fungal relationship (parasitism).

The continuum concept remains a useful framework for studying mycorrhizal functioning

Recent studies have questioned the validity of the mutualism-parasitism continuum of mycorrhizal function. This paper re-evaluates the continuum model and analyzes these concerns. Three insights arise from this analysis. First, the continuum model defines mycorrhizal function as an emergent property of complex interactions. The model identifies resource trade and symbiotic control as key determinants of the costs and benefits of the symbiosis for plants and fungi, and the interaction of these factors with the environment ultimately controls mycorrhizal function. Second, analysis of carbon costs and phosphorus benefits is too narrow a focus to accurately predict mycorrhizal function. Analysis of plant and fungal fitness responses in ecologically and evolutionarily relevant systems are required to elucidate the full range of nutritional and non-nutritional factors embodied within mycorrhizal functioning. Finally, the definition of the term ‘parasitism’ has evolved. Some fields of science maintain the original definition of a nutritional relationship between host and parasite while other fields define it as a +/- fitness relationship. This has generated debate about whether the continuum of mycorrhizal functioning should properly be called a positive–negative response continuum or a mutualism-parasitism continuum. This controversy about semantics should be resolved, but it does not overturn the continuum concept.

The Effect of Mycorrhizae on Plant Growth and Reproduction Varies with Soil Phosphorus and Developmental Stage

Abstract Determining the impact of both environmental variation and developmental stage on plant-mycorrhizal associations is important, as both can shift the association along the mutualism-parasitism continuum. This study examines the effect of phosphorus level on the response of Allium vineale to mycorrhizae across all plant life stages, including plant fecundity and the relative allocation of resources to three different reproductive modes (flowers, asexual underground offsets, and asexual aerial bulbils). For A. vineale, the impact of mycorrhizae varies significantly with life stage, as an early growth depression at 1 mo was reversed by 15 mo, resulting in mycorrhizal plants having larger bulbs over all P levels and producing more bulbils and larger offsets than nonmycorrhizal plants at lower P levels. However the presence of mycorrhizae did not affect the relative allocation of resources among the three reproductive modes. These results emphasize the importance of long-term studies of plant-mycorrhiz...

The microbe-free plant: fact or artifact?

Plant–microbe interactions are ubiquitous. Plants are threatened by pathogens, but they are even more commonly engaged in neutral or mutualistic interactions with microbes: belowground microbial plant associates are mycorrhizal fungi, Rhizobia, and plant-growth promoting rhizosphere bacteria, aboveground plant parts are colonized by internally living bacteria and fungi (endophytes) and by microbes in the phyllosphere (epiphytes). We emphasize here that a completely microbe-free plant is an exotic exception rather than the biologically relevant rule. The complex interplay of such microbial communities with the host–plant affects multiple vital parameters such as plant nutrition, growth rate, resistance to biotic and abiotic stressors, and plant survival and distribution. The mechanisms involved reach from direct ones such as nutrient acquisition, the production of plant hormones, or direct antibiosis, to indirect ones that are mediated by effects on host resistance genes or via interactions at higher trophic levels. Plant-associated microbes are heterotrophic and cause costs to their host plant, whereas the benefits depend on the current environment. Thus, the outcome of the interaction for the plant host is highly context dependent. We argue that considering the microbe-free plant as the “normal” or control stage significantly impairs research into important phenomena such as (1) phenotypic and epigenetic plasticity, (2) the “normal” ecological outcome of a given interaction, and (3) the evolution of plants. For the future, we suggest cultivation-independent screening methods using direct PCR from plant tissue of more than one fungal and bacterial gene to collect data on the true microbial diversity in wild plants. The patterns found could be correlated to host species and environmental conditions, in order to formulate testable hypotheses on the biological roles of plant endophytes in nature. Experimental approaches should compare different host–endophyte combinations under various relevant environmental conditions and study at the genetic, epigenetic, transcriptional, and physiological level the parameters that cause the interaction to shift along the mutualism–parasitism continuum.

A novel reef coral symbiosis

Reef building corals form close associations with unicellular microalgae, fungi, bacteria and archaea, some of which are symbiotic and which together form the coral holobiont. Associations with multicellular eukaryotes such as polychaete worms, bivalves and sponges are not generally considered to be symbiotic as the host responds to their presence by forming physical barriers with an active growth edge in the exoskeleton isolating the invader and, at a subcellular level, activating innate immune responses such as melanin deposition. This study describes a novel symbiosis between a newly described hydrozoan (Zanclea margaritae sp. nov.) and the reef building coral Acropora muricata (=A. formosa), with the hydrozoan hydrorhiza ramifying throughout the coral tissues with no evidence of isolation or activation of the immune systems of the host. The hydrorhiza lacks a perisarc, which is typical of symbiotic species of this and related genera, including species that associate with other cnidarians such as octocorals. The symbiosis was observed at all sites investigated from two distant locations on the Great Barrier Reef, Australia, and appears to be host species specific, being found only in A. muricata and in none of 30 other species investigated at these sites. Not all colonies of A. muricata host the hydrozoans and both the prevalence within the coral population (mean = 66%) and density of emergent hydrozoan hydranths on the surface of the coral (mean = 4.3 cm−2, but up to 52 cm−2) vary between sites. The form of the symbiosis in terms of the mutualism–parasitism continuum is not known, although the hydrozoan possesses large stenotele nematocysts, which may be important for defence from predators and protozoan pathogens. This finding expands the known A. muricata holobiont and the association must be taken into account in future when determining the corals’ abilities to defend against predators and withstand stress.

Evolution of mycoheterotrophy in plants: a phylogenetic perspective

Evolution of mycoheterotrophy in plants: a phylogenetic perspective