Microbiota manipulation through the secretion of effector proteins is fundamental to the wealth of lifestyles in the fungal kingdom

Abstract

Abstract Fungi are well-known decomposers of organic matter that thrive in virtually any environment on Earth where they encounter wealths of other microbes. Some fungi evolved symbiotic lifestyles, including pathogens and mutualists, that have mostly been studied in binary interactions with their hosts. However, we now appreciate that such interactions are greatly influenced by the ecological context in which they take place. While establishing their symbioses, fungi not only interact with their hosts but also with the host-associated microbiota. Thus, they target the host and its associated microbiota as a single holobiont. Recent studies have shown that fungal pathogens manipulate the host microbiota by means of secreted effector proteins with selective antimicrobial activity to stimulate disease development. In this review, we discuss the ecological contexts in which such effector-mediated microbiota manipulation is relevant for the fungal lifestyle and argue that this is not only relevant for pathogens of plants and animals but also beneficial in virtually any niche where fungi occur. Moreover, we reason that effector-mediated microbiota manipulation likely evolved already in fungal ancestors that encountered microbial competition long before symbiosis with land plants and mammalian animals evolved. Thus, we claim that effector-mediated microbiota manipulation is fundamental to fungal biology.