The rise and rise of emerging infectious fungi challenges food security and ecosystem health

This article highlights some of the more notable persistent fungal diseases of our times. It draws attention to the emergence of new fungal pathotypes infecting food staple crops, due largely to modern agricultural practices, and to nascent fungal diseases decimating frog populations worldwide and killing hibernating bats in Northern USA. We invoke use of the basic disease triangle concept to highlight the “missing” data, with regards to pathogen and host biology and to the various environmental parameters which may dictate disease spread. Given these data “voids” we comment on the implementation of policy. We conclude with a series of recommendations for improved disease surveillance and reporting, the need for greater public awareness of these issues and a call for greater funding for fungal research. In so doing, we have exploited Magnaporthe oryzae and Batrachochytrium dendrobatidis as exemplar emerging infectious fungi. Our aim is to highlight the impact of emerging and emergent fungi on food security and, more broadly, ecosystem health.     

Trichoderma/pathogen/plant interaction in pre-harvest food security

Large losses before crop harvesting are caused by plant pathogens, such as viruses, bacteria, oomycetes, fungi, and nematodes. Among these, fungi are the major cause of losses in agriculture worldwide. Plant pathogens are still controlled through application of agrochemicals, causing human disease and impacting environmental and food security. Biological control provides a safe alternative for the control of fungal plant pathogens, because of the ability of biocontrol agents to establish in the ecosystem. Some Trichoderma spp. are considered potential agents in the control of fungal plant diseases. They can interact directly with roots, increasing plant growth, resistance to diseases, and tolerance to abiotic stress. Furthermore, Trichoderma can directly kill fungal plant pathogens by antibiosis, as well as via mycoparasitism strategies. In this review, we will discuss the interactions between Trichoderma/fungal pathogens/plants during the pre-harvest of crops. In addition, we will highlight how these interactions can influence crop production and food security. Finally, we will describe the future of crop production using antimicrobial peptides, plants carrying pathogen-derived resistance, and plantibodies.     

Deciphering microbial landscapes of fish eggs to mitigate emerging diseases

Animals and plants are increasingly suffering from diseases caused by fungi and oomycetes. These emerging pathogens are now recognized as a global threat to biodiversity and food security. Among oomycetes, Saprolegnia species cause significant declines in fish and amphibian populations. Fish eggs have an immature adaptive immune system and depend on nonspecific innate defences to ward off pathogens. Here, meta-taxonomic analyses revealed that Atlantic salmon eggs are home to diverse fungal, oomycete and bacterial communities. Although virulent Saprolegnia isolates were found in all salmon egg samples, a low incidence of Saprolegniosis was strongly correlated with a high richness and abundance of specific commensal Actinobacteria, with the genus Frondihabitans (Microbacteriaceae) effectively inhibiting attachment of Saprolegniato salmon eggs. These results highlight that fundamental insights into microbial landscapes of fish eggs may provide new sustainable means to mitigate emerging diseases.     

Crown closure affects endophytic leaf mycobiome compositional dynamics over time in Pseudotsuga menziesii var. menziesii

Old-growth Pseudotsuga menziesii var. menziesii forests produce complex environmental and spatial gradients along which biota assemble. Given this, it has been proposed that changes in the crown microenvironment are associated with different community assembly outcomes for needle fungi. Using high-throughput sequencing, the endophytic mycobiomes of needles were characterized for increasing ages of needles sampled along the boles of eight coastal Douglas-fir trees. Leveraging airborne light detection and ranging (LiDAR) data to create three-dimensional “point cloud” representations of tree crowns revealed that crown closure accounted for more fungal compositional variation than height in crown, and fungal richness and diversity were positively correlated with increasing crown closure. Supplementing the point clouds of each climbed tree with clouds from >5,000 randomly selected trees in the study area showed that fungal communities from closed portions of the crown were increasingly structured with needle age. These findings highlight the importance of the crown microenvironment in the development of foliar fungal communities for a foundation tree species.     

Antioxidants and iron chelators inhibit oxygen radical generation in fungal cultures of plant pathogenic fungi

Eutypa dieback and Esca are serious fungal grapevine trunk diseases (GTDs). Eutypa dieback is caused by Eutypa lata (Elata), and is often associated Phaeoacremonium minimum (Pmin), and Phaeomoniella chlamydospora (Pch) which are also important contributors to Esca disease.Understanding the complex pathogenesis mechanisms used by these causative fungi may potentially lead targeted treatments for GTDs in the future. Elata has been reported as a wood decay “soft rot” fungus and understanding of Elata’s pathogenesis chemistries can aid in controlling GTDs. Recent work that suggests that Pmin and Pch may contribute to pathogenesis by stimulating hydroxyl radical generation via secretion of low molecular weight phenolic metabolites. Building on these findings, we tested a hypothesis that antioxidants and chelators, and biocontrol agents that have been reported to secrete antioxidants and low molecular weight chelators, may inhibit the growth and activity of these fungi. Butylated hydroxy anisole (BHA) and butylated hydroxytoluene (BHT) were tested as antioxidant/chelators. BHA was found to be a highly effective control measure for the three pathogenic fungi tested at concentrations >0.5 mM. The biocontrol species Bacillus subtilis and Hypocrea (Trichoderma) atroviride were also tested, with both H. atroviride and B. subtilis effectively inhibiting growth of the three GTD fungi.     

Influence of fungal isolates infecting tall fescue on multitrophic interactions

The epichloae are ascomycetous fungi in the genera Epichloë and Neotyphodium that live within grasses. Some of these fungi produce alkaloids that can help protect the host from herbivores. The alkaloids may also travel up the food web and affect members of the third trophic level. In this way they can produce trophic cascades which are rippling effects when a trophic level impacts those above or below it. We briefly summarize the general patterns of multitrophic effects of endophytes and highlight the most recent studies on this topic. Further, we report on our study in which we tested if different fungal strains in tall fescue (cultivar Jesup) affect multitrophic interactions involving aphids and their parasitoid natural enemies. Using both the common strain of N. coenophialum and a novel isolate (AR577), we allowed potted plants to be colonized by aphids and parasitoids in a semi-natural setting. We found that endophyte infection of tall fescue resulted in greater vegetative growth of the plant. We also found that N. coenophialum modified bottom-up cascades by depressing both aphid and parasitoid densities. Finally, we found that multitrophic effects were modified by fungal isolate: the common strain had stronger negative impacts on aphid and parasitoid densities than did the novel isolate.     

Plant resistance signalling hijacked by a necrotrophic fungal pathogen

The strategies used by necrotrophic fungal pathogens to infect plants are often perceived as lacking the sophistication of their haustorium producing, host defence suppressing, biotrophic counterparts. There is also a relative paucity of knowledge regarding how effective gene-for-gene based resistance reactions might function against necrotrophic plant pathogens. However, recent data has emerged from a number of systems which has highlighted that particular species of necrotrophic (and/or hemibiotrophic) fungi, have evolved very sophisticated strategies for plant infection which appear, in fact, to hijack the host resistance responses that are commonly deployed against biotrophs. Both disease resistance (R) protein homologues and mitogen-activated protein kinase (MAPK) cascades commonly associated with incompatible disease resistance responses; appear to be targeted by necrotrophic fungi during compatible disease interactions. These findings highlight an emerging sophistication in the strategies deployed by necrotrophic fungi to infect plants.Key words: Mycosphaerella graminicola, Septoria tritici, Triticum aestivum, mitogen-activated protein kinase, programmed cell death, fungal pathogen, disease resistance, disease susceptibility, toxin     

Actividad de la micafungina contra las biopelículas de Candida

BackgroundMost recalcitrant infections are associated to colonization and microbial biofilm development. These biofilms are difficult to eliminate by the immune response mechanisms and the current antimicrobial therapy.AimTo describe the antifungal of micafungin against fungal biofilms based in the scientific and medical literature of recent years.MethodsWe have done a bibliographic retrieval using the scientific terms “micafungin”, “activity”, “biofilm”, “Candida”, “Aspergillus”, “fungi”, “mycos”*, susceptibility, in PubMed/Medline from the National Library of Medicine from 2006 to 2009.ResultsMost current antifungal agents (amphotericin B and fluconazole) and the new azole antifungals have no activity against fungal biofilms. However, micafungin and the rest of echinocandins are very active against Candida albicans, Candida dubliniensis, Candida glabrata, and Candida krusei biofilms but their activities are variable and less strong against Candida tropicalis and Candida parapsilosis biofilms. Moreover, they have not activities against the biofilms of Cryptococcus y Trichosporon.ConclusionsThe activity of micafungin against Candida biofilms gives more strength to its therapeutic indication for candidaemia and invasive candidiasis associated to catheter, prosthesis and other biomedical devices.     

Studying fungal pathogens of humans and fungal infections: fungal diversity and diversity of approaches

Seminal work by Louis Pasteur revealed the contribution of fungi – yeasts and microsporidia to agroindustry and disease in animals, respectively. More than 150 years later, the impact of fungi on human health and beyond is an ever-increasing issue, although often underestimated. Recent studies estimate that fungal infections, especially those caused by Candida, Cryptococcus and Aspergillus species, kill more than one million people annually. Indeed, these neglected infections are in general very difficult to cure and the associated mortality remains very high even when antifungal treatments exist. The development of new antifungals and diagnostic tools that are both necessary to fight fungal diseases efficiently, requires greater insights in the biology of the fungal pathogens of humans in the context of the infection, on their epidemiology, and on their role in the human mycobiota. We also need a better understanding of the host immune responses to fungal pathogens as well as the genetic basis for the increased sensitivity of some individuals to fungal infections. Here, we highlight some recent progress made in these different areas of research, in particular based on work conducted in our own laboratories. These progresses should lay the ground for better management of fungal infections, as they provide opportunities for better diagnostic, vaccination, the development of classical antifungals but also strategies for targeting virulence factors or the host.     

Predicting disease occurrence with high accuracy based on soil macroecological patterns of Fusarium wilt

Soil-borne plant diseases are increasingly causing devastating losses in agricultural production. The development of a more refined model for disease prediction can aid in reducing crop losses through the use of preventative control measures or soil fallowing for a planting season. The emergence of high-throughput DNA sequencing technology has provided unprecedented insight into the microbial composition of diseased versus healthy soils. However, a single independent case study rarely yields a general conclusion predictive of the disease in a particular soil. Here, we attempt to account for the differences among various studies and plant varieties using a machine-learning approach based on 24 independent bacterial data sets comprising 758 samples and 22 independent fungal data sets comprising 279 samples of healthy or Fusarium wilt-diseased soils from eight different countries. We found that soil bacterial and fungal communities were both clearly separated between diseased and healthy soil samples that originated from six crops across nine countries or regions. Alpha diversity was consistently greater in the fungal community of healthy soils. While diseased soil microbiomes harbored higher abundances of Xanthomonadaceae, Bacillaceae, Gibberella, and Fusarium oxysporum, the healthy soil microbiome contained more Streptomyces Mirabilis, Bradyrhizobiaceae, Comamonadaceae, Mortierella, and nonpathogenic fungi of Fusarium. Furthermore, a random forest method identified 45 bacterial OTUs and 40 fungal OTUs that categorized the health status of the soil with an accuracy >80%. We conclude that these models can be applied to predict the potential for occurrence of F. oxysporum wilt by revealing key biological indicators and features common to the wilt-diseased soil microbiome.Subject terms: Molecular ecology, Infectious-disease diagnostics     

Root endophyte symbiosis in vitro between the ectomycorrhizal basidiomycete Tricholoma matsutake and the arbuscular mycorrhizal plant Prunus speciosa

We previously reported that Tricholoma matsutake and Tricholoma fulvocastaneum, ectomycorrhizal basidiomycetes that associate with Pinaceae and Fagaceae, respectively, in the Northern Hemisphere, could interact in vitro as a root endophyte of somatic plants of Cedrela odorata (Meliaceae), which naturally harbors arbuscular mycorrhizal fungi in South America, to form a characteristic rhizospheric colony or “shiro”. We questioned whether this phenomenon could have occurred because of plant–microbe interactions between geographically separated species that never encounter one another in nature. In the present study, we document that these fungi formed root endophyte interactions and shiro within 140 days of inoculation with somatic plants of Prunus speciosa (=Cerasus speciosa, Rosaceae), a wild cherry tree that naturally harbors arbuscular mycorrhizal fungi in Japan. Compared with C. odorata, infected P. speciosa plants had less mycelial sheath surrounding the exodermis, and the older the roots, especially main roots, the more hyphae penetrated. In addition, a large number of juvenile roots were not associated with hyphae. We concluded that such root endophyte interactions were not events isolated to the interactions between exotic plants and microbes but could occur generally in vitro. Our pure culture system with a somatic plant allowed these fungi to express symbiosis-related phenotypes that varied with the plant host; these traits are innately programmed but suppressed in nature and could be useful in genetic analyses of plant–fungal symbiosis.     

Potential impact of climate change on fungal distributions: analysis of 2 years of contrasting weather in the UK

The impact of climate change on fungal growth and spore production is less well documented than for allergenic pollen grains, although similar implications for respiratory tract diseases in humans occur. Fungal spores are commonly described as either “dry” or “wet” according to the type of weather associated with their occurrence in the air. This study examined the distribution of selected fungal spores (Alternaria spp., Cladosporium spp., Didymella spp., Epicoccum spp., Leptosphaeria spp. and rusts) occurring in the West Midlands of UK during 2 years of contrasting weather. Spore specimens were collected using a 7-day volumetric air sampler and then analysed with the aid of light microscopy. Distributions of spores were then studied using normality tests and Mann–Whitney U test, while relationships with meteorological parameters were investigated using Spearman’s rank test and angular-linear correlation for wind direction analysis. Our results showed that so-called wet spores were more sensitive to the weather changes showing statistically significant differences between the 2 years of study, in contrast to “dry” spores. We predict that in following years we will observe accelerated levels in allergenic fungal spore production as well as changes in species diversity. This study could be a starting point to revise the grouping system of fungal spores as either “dry” or “wet” types and their response to climate change.     

Fire and local factors shape ectomycorrhizal fungal communities associated with Pinus ponderosa in mountains of the Madrean Sky Island Archipelago

With a warming and drying climate, coniferous forests worldwide are increasingly threatened by wildfires. We examined how fire impacts ectomycorrhizal (EM) fungi associated with Pinus ponderosa, an important tree species in western North America. In the biodiverse Madrean Sky Islands, P. ponderosa forests exist on insular mountains separated by arid lands. How do EM fungi in these isolated ranges respond to fire, and can data from individual ranges predict community shifts after fire at a regional scale? By comparing areas in two ranges that experienced moderate fires 12–16 y earlier, and proximate areas in each range without recent fire, we reveal pervasive effects on diversity and composition of EM communities more than a decade after moderate fires occurred. Post-fire differences in EM communities in different ranges highlight the challenge of predicting fungal community shifts in these isolated forests, despite similarities of climate, plant communities, and fire severity.     

Novel and unique domains in aminoacyl-tRNA synthetases from human fungal pathogens Aspergillus niger,Candida albicans and Cryptococcus neoformans

Background

Some species of fungi can cause serious human diseases, particularly to immuno-compromised individuals. Opportunistic fungal infections are a leading cause of mortality, and present an emerging challenge that requires development of new and effective therapeutics. Aminoacyl-tRNA synthetases (aaRSs) are indispensable components of cellular protein translation machinery and can be targeted for discovery of novel anti-fungal agents.

Results

Validation of aaRSs as potential drug targets in pathogenic microbes prompted us to investigate the genomic distribution of aaRSs within three fungi that infect humans – A. niger, C. albicans and C. neoformans. Hidden Markov Models were built for aaRSs and related proteins to search for homologues in these fungal genomes. Here, we provide a detailed and comprehensive annotation for 3 fungal genome aaRSs and their associated proteins. We delineate predicted localizations, subdomain architectures and prevalence of unusual motifs within these aaRSs. Several fungal aaRSs have unique domain appendages of unknown function e.g. A. niger AsxRS and C. neoformans TyrRS have additional domains that are absent from human homologs.

Conclusions

Detailed comparisons of fungal aaRSs with human homologs suggest key differences that could be exploited for specific drug targeting. Our cataloging and structural analyses provide a comprehensive foundation for experimentally dissecting fungal aaRSs that may enable development of new anti-fungal agents.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-1069) contains supplementary material, which is available to authorized users.     

Large‐scale molecular genetic analysis in plant‐pathogenic fungi: a decade of genome‐wide functional analysis

Plant‐pathogenic fungi cause diseases to all major crop plants world‐wide and threaten global food security. Underpinning fungal diseases are virulence genes facilitating plant host colonization that often marks pathogenesis and crop failures, as well as an increase in staple food prices. Fungal molecular genetics is therefore the cornerstone to the sustainable prevention of disease outbreaks. Pathogenicity studies using mutant collections provide immense function‐based information regarding virulence genes of economically relevant fungi. These collections are rich in potential targets for existing and new biological control agents. They contribute to host resistance breeding against fungal pathogens and are instrumental in searching for novel resistance genes through the identification of fungal effectors. Therefore, functional analyses of mutant collections propel gene discovery and characterization, and may be incorporated into disease management strategies. In the light of these attributes, mutant collections enhance the development of practical solutions to confront modern agricultural constraints. Here, a critical review of mutant collections constructed by various laboratories during the past decade is provided. We used Magnaporthe oryzae and Fusarium graminearum studies to show how mutant screens contribute to bridge existing knowledge gaps in pathogenicity and fungal–host interactions.