Marine fungal traits: towards a functional understanding of pelagic fungal ecology

Abstract

Fungal life has been detected in practically every ecosystem explored to date, amounting to an estimated 12 Gt C or 2% of the total biomass on Earth. Fungi fulfil a number of functional roles in terrestrial ecosystem processes, through the decomposition of complex organic matter, remineralisation of carbon and other nutrients, and various interactions with other organisms. Marine environments harbour phylogenetically diverse fungal communities, including many taxa also found on land, but comparatively little is known about the functional ecology of marine fungi, particularly in the pelagic open ocean. DNA-based studies have demonstrated spatial and temporal variability in pelagic fungal abundance and community composition, correlating with multiple environmental factors including phytoplankton abundance, temperature, oxygen and nutrient concentrations. However, physiological evidence of pelagic fungal growth responses to changing conditions is currently lacking, precluding the establishment of mechanistic relationships between environmental gradients, pelagic fungal activity, and ecosystem function. This thesis aims to develop a functional understanding of pelagic marine fungal ecology, drawing upon existing functional trait-based approaches from terrestrial fungal and marine plankton ecology. A combination of culture-dependent and independent methods are applied to investigate fungal diversity and activity throughout the water column at the Porcupine Abyssal Plain Sustained Observatory (PAP-SO) – an open ocean site in the North-East Atlantic. Environmentally relevant pelagic fungal isolates are selected based on their in situ activity and cultured under a range of experimental conditions in the laboratory to characterise their physiological and morphological traits. Growth responses to variable conditions are compared between isolates and between taxa, with the aim of identifying general, predictable patterns of pelagic fungal trait variation along environmental gradients. Pelagic fungal isolates demonstrate physiological and morphological plasticity in response to variable temperature, salinity and resource availability. Filamentous isolates vary in colony extension rate and mycelial density, with a temperature-dependent rate-density relationship. Yeast-like isolates vary in growth rate and biomass yield, with a temperature-dependent rate-yield relationship. Salinity and carbon substrate responses are relatively isolate-specific. Unicellular yeast Naganishia diffluens, active throughout the water column at PAP-SO, is able to utilise a broad diversity of nitrogen sources including nitrate, and responds to low nitrogen availability by decreasing in growth rate and cell size. Polymorphic yeast Aureobasidium pullulans only develops filamentous growth at high substrate concentrations, while budding yeast-type cells also show dynamic size and shape responses to substrate availability. This work provides novel insight into the ecophysiology of pelagic marine fungi, highlighting the potential for fungal activity, and therefore ecological and biogeochemical functions, to vary along environmental gradients in the ocean.

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ORCID for Poppy Joanne Diver: orcid.org/0000-0002-9949-8392

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