Fantastic Antagonists and Where to Find Them: The Global Distribution of Nematode-Antagonistic Fungi

Under specific conditions, plant-parasitic nematodes can be suppressed by antagonistic members of the local soil microbiome. Although fungal nematode antagonists are regularly detected in soils worldwide, their global distribution has not been systematically documented. We mined a global fungal dataset comprising nearly 28,000 samples from 484 studies focusing on biomes and sample types that might comprise nematode antagonists. After selecting DNA read data that allowed for fungal identification until the species level, we showed that 82.6% of the soil samples contained one or more nematode antagonist. Antagonist presence differed among biomes; the probability of detecting antagonists was highest in croplands and other anthropogenically disturbed biomes (86%), whereas samples from deserts and tundra showed relatively low detection probability (respectively 20% and 6%). Our analyses revealed that most of the common nematode antagonists show barely any biogeography; their presence in all continents underlines the enormous ecological flexibility of these fungal species. Remarkably, half of fungal antagonist species present in a selection of the six most common taxa across all biomes, were also most prevalent in a single biome, croplands. With one exception, Chaetomium globosum, the most frequently detected antagonistic fungi belonged to a single fungal order, the Hypocreales. These common and widespread nematode antagonists all parasitize representatives of fungi and insects as well. Next, we also investigated the commonness and the global distribution of microbial antagonists that are frequently applied as biological control agents against plant-parasitic nematodes. Species such as Purpureocillium lilacinum, Metacordyceps chlamydosporium and Trichoderma harzianum were detected in 6 - 23% of the cropland samples, and occurred on all continents. Analysis of the impact of mean annual temperature and annual precipitation on the most common nematode antagonists in croplands revealed that, except for Trichoderma asperellum, all were promoted by higher temperatures, and inhibited by higher annual precipitation. Insights in the prevalence and the distribution of specific and non-specific nematode antagonists at a global scale, especially in croplands, might contribute to the exploration of the nematode-suppressive potential that is more common than often assumed.