EVs in fungal biofilm biology
Membrane vesicles play a significant role in the formation and
maintenance of fungal biofilms (Zarnowski et al., 2018; Zarnowski et
al., 2022). Biofilms are complex structures composed of communities of
sessile cells embedded in a self-produced extracellular matrix (ECM)
(Ramage et al., 2009; Harding et al., 2009). Formation of biofilms
generally involves a succession of phases commencing with adherence of
cells to surfaces, followed by the growth of cells which are covered by
the ECM, leading up to maturation and dispersal of cells (Chandra et
al., 2001; Harding et al., 2009). Nonetheless, the exact mechanisms by
which membrane vesicles contribute to biofilm formation are not fully
understood, but several mechanisms have been proposed. One proposed
mechanism is that membrane vesicles are involved in the secretion of
extracellular matrix (ECM) components, such as polysaccharides and
proteins, which are necessary for the formation of the biofilm structure
(Harding et al., 2009; Di Martino, 2018). Vesicles are also known to
transport enzymes that are involved in the degradation of host tissues,
which can create a suitable environment for biofilm formation
(Zarnowskiet al., 2018). Another proposed mechanism is that membrane vesicles are
involved in intercellular communication within the biofilm. Studies have
shown that vesicles can transfer signaling molecules, such as
lipopeptides and small RNAs, between cells, which can coordinate the
behavior of the cells within the biofilm (Leone et al., 2017).
Additionally, membrane vesicles are also thought to play a role in the
development of antifungal resistance. Vesicles have been found to
sequester drugs and protect the biofilm cells from their effects, and
also to detoxify drugs, breaking them down before they reach the cells (
et
al., 2018; Zarnowski et al., 2022).
EVs are also involved in development of biofilms of some bacterial and
yeast species (i.e., Toxoplasma gondii etc. ) (Li et al., 2018,
Zarnowski et al., 2022). Studies on the role of EV in biofilms in plant
filamentous plant fungi have not been reported, although in yeasts
(e.g., C. albicans ) a number of studies have been conducted.
Recent studies have shown that the structural complexity of biofilms
(i.e., high cell density, ECM etc.) leads to production of EVs which can
enhance drug resistance and are unique to planktonic (Free-living) cells
(Bielska and May, 2019, Honorato et al., 2021, Zarnowski et al., 2022).
The cargo of C. albicans biofilm EVs ferry compounds including
cell-wall degrading enzymes as well as mannan and glucan (Zarnowski et
al., 2014, Mitchell et al., 2015, Garcia-Ceron et al., 2021). Compatible
with the assembly of the ECM, the delivery mannan-glucan complex by EVs
is critical for drug resistance (Zarnowski et al., 2014, Mitchell et
al., 2015). ESCRT-I genes including Hse1 and Vps27 were found enclosed
in secreted EV cargo of C. albicans . These ESCRT-I containing EVs
are reported to restore the biofilm matrix architecture and quantities
of the key mannan–glucan components, an indication that they may
function in biofilm EV production and promotion of matrix biogenesis
(Zarnowski et al., 2018). EVs are also believed to control morphogenesis
in C. albicans as their presence hinders the process of biofilm
formation and dimorphic transition (Honorato et al., 2021). For
instance, EVs containing RNA are assumed to actively take part in the
dimorphic transition of Pichia fermentans (Leone et al., 2017).
Overall, membrane vesicles are involved in multiple aspects of biofilm
formation, including the secretion of matrix components, intercellular
communication, and drug resistance.