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

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 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.

A highly polymorphic effector protein promotes fungal virulence through suppression of plant-associated Actinobacteria

“…Interestingly, some of these effectors impact growth of Actinobacterial keystone taxa of the Arabidopsis phyllosphere in vitro , suggesting that the suppression of Actinobacteria in host microbiota might be a strategy adopted by diverse microbial plant pathogens. These findings furthermore support the hypothesis that effector-mediated manipulation of host microbiota communities may be a widely deployed strategy of plant pathogens to support host colonization (Snelders et al ., 2022).…”

“…However, novel effector functions are still discovered. For instance, we recently demonstrated that some effectors are secreted to manipulate plant microbiota compositions to promote host colonization (Snelders et al, 2020(Snelders et al, , 2021(Snelders et al, , 2022.…”

A highly polymorphic effector protein promotes fungal virulence through suppression of plant‐associated Actinobacteria

“…Interestingly, some of these effectors impact the growth of Actinobacterial keystone taxa of the Arabidopsis phyllosphere in vitro , suggesting that the suppression of Actinobacteria in host microbiota might be a strategy adopted by diverse microbial plant pathogens. These findings furthermore support the hypothesis that effector‐mediated manipulation of host microbiota communities may be a widely deployed strategy of plant pathogens to support host colonization (Snelders et al ., 2022).…”

Fungal Effectoromics: A World in Constant Evolution

“…In each ecological interaction, communication exists between effectors and receptors that shape the outcome of the interaction. Although widely associated with pathogenicity, effectors have been discovered in plant-beneficial organisms such as mutualist mycorrhizal species and endophytes [ 13 , 14 , 15 , 16 ] and the study of their roles in microbe-microbe interactions is gaining traction in the field of effector biology [ 17 , 18 ]. These molecules are ubiquitous in microorganisms, and the effectorome complement of each organism is highly specialized and greatly affects its lifestyle, as both gene gain and loss of certain effectors have implications for pathogen virulence and host adaptation [ 19 , 20 , 21 , 22 ].…”