Good neighbors aplenty: fungal endophytes rarely exhibit competitive exclusion patterns across a span of woody habitats

Abstract

Environmental forces and biotic interactions, both positive and negative, structure ecological communities, but their relative roles remain obscure despite strong theory. For instance, ecologically similar species, based on the principle of limiting similarity, are expected to be most competitive and show negative interactions. Specious communities that assemble along broad environmental gradients afford the most power to test theory, but the communities often are difficult to quantify. Microbes, specifically fungal endophytes of wood, are especially suited for testing community assembly theory because they are relatively easy to sample across a comprehensive range of environmental space with clear axes of variation. Moreover, endophytes mediate key forest carbon cycle processes, and although saprophytic fungi from dead wood typically compete, endophytic fungi in living wood may enhance success through cooperative symbioses. To classify interactions within endophyte communities, we analyzed fungal DNA barcode variation across 22 woody plant species growing in woodlands near Richmond, New South Wales, Australia. We estimated the response of endophytes to the measured wood environment (i.e., 11 anatomical and chemical wood traits) and each other using latent‐variable models and identified recurrent communities across wood environments using model‐based classification. We used this information to evaluate whether (1) co‐occurrence patterns are consistent with strong competitive exclusion, and (2) a priori classifications by trophic mode and phylum distinguish taxa that are more likely to have positive vs. negative associations under the principle of limiting similarity. Fungal endophytes were diverse (mean = 140 taxa/sample), with differences in community composition structured by wood traits. Variation in wood water content and carbon concentration were associated with especially large community shifts. Surprisingly, after accounting for wood traits, fungal species were still more than three times more likely to have positive than negative co‐occurrence patterns. That is, patterns consistent with strong competitive exclusion were rare, and positive interactions among fungal endophytes were more common than expected. Confirming the frequency of positive vs. negative interactions among fungal taxa requires experimental tests, and our findings establish clear paths for further study. Evidence to date intriguingly suggests that, across a wide range of wood traits, cooperation may outweigh combat for these fungi.

Empirical Support for the Pattern of Competitive Exclusion between Insect Parasitic Fungi

“…Ascomycete insect pathogens are closely related to plant pathogens and endophytes [ 42 ]. The DNA barcoding analysis of wood endophytes revealed that CEP was not applicable to these fungi since diverse fungal taxa were co-present in wood samples [ 43 ]. Instead, the model of competition–colonization tradeoffs has been suggested to mediate the competition and coexistence of the fungal mycorrhiza or pathogens since the diverse species of these fungi could either occupy different root tips [ 13 , 44 , 45 ] or infect different parts of individual plants [ 34 , 36 ].…”

Wood construction more strongly shapes deadwood microbial communities than spatial location over 5 years of decay

“…Globally, microbes are the key decay agents but their decay abilities are shaped by environmental conditions and biotic interactions. To date, we have had a poor understanding of what regulates wood‐decay community structure and function through time (Lee et al ., 2019). This study shows that environmental factors that predict decay rates (Zanne et al ., 2015) have the same rank importance in structuring deadwood microbial communities in a temperate deciduous oak‐hickory forest.…”

Mollisiaceae: An overlooked lineage of diverse endophytes

“…While generally considered to be “just” saprotrophs, some studies also report Mollisia as endophytes of leaves and twigs in diverse host plants ( Sieber, 1989 , Barklund and Kowalski, 1996 , Shamoun and Sieber, 2000 , Kowalski and Andruch, 2012 , Anderson Stewart et al. 2019 , Lee et al. 2019 ).…”