Context-dependent symbioses and their potential roles in wildlife diseases

Daskin, Joshua H.; Alford, Ross A.

doi:10.1098/rspb.2011.2276

Cited by 77 publications

(68 citation statements)

References 96 publications

(146 reference statements)

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“…Context dependency is common in both the establishment and maintenance of many facultative fungal symbioses and in the functional outcomes of such associations (43)(44)(45)(46)(47) and likely shapes the success of EHB-fungal encounters in nature. Our results reveal that nutrient conditions can be important for successful reassociations.…”

Section: Discussionmentioning

confidence: 99%

Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations

Arendt

Hockett

Araldi-Brondolo

et al. 2016

Appl Environ Microbiol

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bEndohyphal bacteria (EHB) can influence fungal phenotypes and shape the outcomes of plant-fungal interactions. Previous work has suggested that EHB form facultative associations with many foliar fungi in the Ascomycota. These bacteria can be isolated in culture, and fungi can be cured of EHB using antibiotics. Here, we present methods for successfully introducing EHB into axenic mycelia of strains representing two classes of Ascomycota. We first establish in vitro conditions favoring reintroduction of two strains of EHB (Luteibacter sp.) into axenic cultures of their original fungal hosts, focusing on fungi isolated from healthy plant tissue as endophytes: Microdiplodia sp. (Dothideomycetes) and Pestalotiopsis sp. (Sordariomycetes). We then demonstrate that these EHB can be introduced into a novel fungal host under the same conditions, successfully transferring EHB between fungi representing different classes. Finally, we manipulate conditions to optimize reintroduction in a focal EHB-fungal association. We show that EHB infections were initiated and maintained more often under low-nutrient culture conditions and when EHB and fungal hyphae were washed with MgCl 2 prior to reassociation. Our study provides new methods for experimental assessment of the effects of EHB on fungal phenotypes and shows how the identity of the fungal host and growth conditions can define the establishment of these widespread and important symbioses.A s appreciation for their diversity and importance grows, plant microbiomes are increasingly of interest for diverse medical, industrial, and agricultural applications (1, 2). However, many plant-associated microbes remain undescribed (3, 4) and/or are found in association with, or as symbionts of, other microorganisms (5-14, 49-52). One example of these microbial symbioses is that between plant-associated fungi and their bacterial endosymbionts (endobacteria, endofungal bacteria, or endohyphal bacteria [EHB]). Recent studies have indicated that EHB are widespread in rhizosphere fungi from diverse fungal phyla (e.g., mycorrhizal and pathogenic fungi from the Basidiomycota, Glomeromycota, and Mucoromycotina [6][7][8][9][10][11][12][13]) and in the highly diverse Ascomycota that infect roots, stems, and leaves as endophytes (14) (class 3 endophytes, sensu [15]). However, functional relationships have been studied for only a few associations, limiting inferences regarding the scope and potential importance of EHB-fungal associations in ecological interactions and human applications (but see references 16 and 17).Most studies aimed at understanding functional relationships between EHB and fungi have focused on root-associated fungi, especially arbuscular mycorrhizal fungi in the Glomeromycota and plant-pathogenic Rhizopus in the Mucoromycotina (6-11, 18-23). EHB in rhizosphere fungi are often vertically transmitted and host specific, and they frequently maintain obligate relationships with their hosts (18)(19)(20). Although EHB can alter the phenotypes of root-associated fungi and profoundly i...

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Section: Discussionmentioning

confidence: 99%

Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations

Arendt

Hockett

Araldi-Brondolo

et al. 2016

Appl Environ Microbiol

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“…Efficient and persistent host and environmental colonization needs to be established: amphibian skin microbiomes are dynamic and can be unstable and unpredictable, and bacterial community composition changes over the animal's lifetime [32]. Bioaugmentation requires a deeper understanding of bacterial community assembly, stability and permeability, couched in the context of amphibian host community, the skin secretions produced by species members of the community and how these are in turn influenced by environmental heterogeneity [39,40]. Probiotics should also exert their beneficial effect across Bd genotypes.…”

Section: Trialled and Testedmentioning

confidence: 99%

Mitigating amphibian chytridiomycoses in nature

Garner

Schmidt²,

Martel

et al. 2016

Phil. Trans. R. Soc. B

135

156

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Amphibians across the planet face the threat of population decline and extirpation caused by the disease chytridiomycosis. Despite consensus that the fungal pathogens responsible for the disease are conservation issues, strategies to mitigate their impacts in the natural world are, at best, nascent. Reducing risk associated with the movement of amphibians, non-amphibian vectors and other sources of infection remains the first line of defence and a primary objective when mitigating the threat of disease in wildlife. Amphibian-associated chytridiomycete fungi and chytridiomycosis are already widespread, though, and we therefore focus on discussing options for mitigating the threats once disease emergence has occurred in wild amphibian populations. All strategies have shortcomings that need to be overcome before implementation, including stronger efforts towards understanding and addressing ethical and legal considerations. Even if these issues can be dealt with, all currently available approaches, or those under discussion, are unlikely to yield the desired conservation outcome of disease mitigation. The decision process for establishing mitigation strategies requires integrated thinking that assesses disease mitigation options critically and embeds them within more comprehensive strategies for the conservation of amphibian populations, communities and ecosystems. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

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“…The fitness impact of services provided by symbiotic interactions on the host is often strongly dependent on the ecological context (Daskin & Alford, 2012). Several studies have shown that the hosts' diet, especially food quality, can be an important influencing factor on interactions between the host and its gut microbiota.…”

Section: Introductionmentioning

confidence: 99%

Food availability affects the strength of mutualistic host–microbiota interactions in Daphnia magna

et al. 2015

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The symbiotic gut microbial community is generally known to have a strong impact on the fitness of its host. Nevertheless, it is less clear how the impact of symbiotic interactions on the hosts' fitness varies according to environmental circumstances such as changes in the diet. This study aims to get a better understanding of host-microbiota interactions under different levels of food availability. We conducted experiments with the invertebrate, experimental model organism Daphnia magna and compared growth, survival and reproduction of conventionalized symbiotic Daphnia with germ-free individuals given varying quantities of food. Our experiments revealed that the relative importance of the microbiota for the hosts' fitness varied according to dietary conditions. The presence of the microbiota had strong positive effects on Daphnia when food was sufficient or abundant, but had weaker effects under food limitation. Our results indicate that the microbiota can be a potentially important factor in determining host responses to changes in dietary conditions. Characterization of the host-associated microbiota further showed that Aeromonas sp. was the most prevalent taxon in the digestive tract of Daphnia.

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Context-dependent symbioses and their potential roles in wildlife diseases

Cited by 77 publications

References 96 publications

Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations

Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations

Mitigating amphibian chytridiomycoses in nature

Food availability affects the strength of mutualistic host–microbiota interactions in Daphnia magna

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