Impact of Fungal Hyphae on Growth and Dispersal of Obligate Anaerobic Bacteria in Aerated Habitats

Abstract

Although a few studies have reported on the presence of anoxic microniches in fungal biofilms, knowledge of the effects of fungal oxygen consumption on bacterial-fungal interactions is limited. Here, we demonstrate the existence and persistence of oxygen-free zones in air-exposed mycelia enabling spore germination, growth, fermentative activity, and dispersal of the obligate anaerobe.

Marine Fungi Select and Transport Aerobic and Anaerobic Bacterial Populations from Polycyclic Aromatic Hydrocarbon-Contaminated Sediments

“…Such an observation further supports that fungi establish specific links with anaerobic bacteria ( 45 ). It is likely that fungi that create anaerobic niches have a crucial role in the organization of microbial communities, playing a key role in the dispersal of anaerobic bacteria ( 75 ). Using time-resolved optical oxygen mapping, microscopy, and metabolite analysis, Xiong et al, for instance, revealed fungal growth-induced formation and persistence of anoxic circum hyphal niches that allowed for spore germination, dispersal, and growth of the obligate anaerobe Clostridium acetobutylicum along hyphae of the litter-decaying fungus Coprinopsis cinerea ( 75 ).…”

“…It is likely that fungi that create anaerobic niches have a crucial role in the organization of microbial communities, playing a key role in the dispersal of anaerobic bacteria ( 75 ). Using time-resolved optical oxygen mapping, microscopy, and metabolite analysis, Xiong et al, for instance, revealed fungal growth-induced formation and persistence of anoxic circum hyphal niches that allowed for spore germination, dispersal, and growth of the obligate anaerobe Clostridium acetobutylicum along hyphae of the litter-decaying fungus Coprinopsis cinerea ( 75 ). Thus, anaerobic conditions created by the fungal growth might allow anaerobic bacteria to survive at the aerobic/anaerobic interface and to overcome hydrocarbon hydrophobic patches in PAH-contaminated sediments.…”

pH Distribution along Growing Fungal Hyphae at Microscale

“…Likewise, such spatial and temporal pH traits may be used to dynamically identify the locations of high enzyme activity along hyphal surfaces. Using oxygen-sensitive particles (Ø: 8 µm), a recent study revealed microscale oxygen heterogeneity in the liquid (~10 µm [ 6 ]) around air-exposed hyphae of C. cinerea [ 6 ]. In our study, we observed 0.7–0.9 units lower and more variable pH values at growing tips than at the more mature hyphal parts ( Figure 4 and Figure S3 ), thereby likely being a driver and result of hyphal elongation, as described by the acid growth hypothesis for plant root and filamentous organisms [ 20 , 53 , 54 ].…”

“…Creating unique and dynamic microenvironments, hyphal surfaces often allow for spatially distinct microbial interactions and functions near and/or affected by hyphae. The hyphosphere [ 1 ] is a zone of fungal activity and a favourable habitat [ 2 , 3 ] for bacterial colonisation and dispersal [ 4 , 5 , 6 ]. As well as oxygen availability [ 6 , 7 ], pH is an important driver for hyphal-bound microbial activity [ 1 ] such as bacterial motility [ 8 ]; degradation of organic matter, lignin and lignocellulose; the mobilisation and transport of nutrients [ 9 , 10 ]; mineral weathering [ 11 ]; and soil structure changes.…”

“…The hyphosphere [ 1 ] is a zone of fungal activity and a favourable habitat [ 2 , 3 ] for bacterial colonisation and dispersal [ 4 , 5 , 6 ]. As well as oxygen availability [ 6 , 7 ], pH is an important driver for hyphal-bound microbial activity [ 1 ] such as bacterial motility [ 8 ]; degradation of organic matter, lignin and lignocellulose; the mobilisation and transport of nutrients [ 9 , 10 ]; mineral weathering [ 11 ]; and soil structure changes. Fungal mycelia typically modulate the environmental pH in their hyphosphere [ 12 , 13 ].…”