FUNCTIONAL BIOLOGY AND ECOLOGY OF PLANKTONIC MARINE FUNGI – Revealing the mechanistic basis of the roles of mycoplankton in the marine carbon cycle | MYCO-CARB | Project | News & Multimedia | H2020 | CORDIS

Periodic Reporting for period 3 - MYCO-CARB (FUNCTIONAL BIOLOGY AND ECOLOGY OF PLANKTONIC MARINE FUNGI – Revealing the mechanistic basis of the roles of mycoplankton in the marine carbon cycle)

Berichtszeitraum: 2021-05-01 bis 2022-10-31

Context: Marine planktonic fungi (mycoplankton) have been largely ignored compared to other plankton groups, such as phytoplankton, especially the roles that they fulfil in marine ecosystems. Recent research has shown that mycoplankton are a structural and functional component of coastal ecosystems that have been almost completely overlooked. Mycoplankton are also likely a substantial proportion of plankton biomass and active particulate organic carbon (POC)-degraders (saprotrophs) in coastal ecosystems. Mycoplankton are also a major plankton group in the open ocean and can dominate on marine snow particles. Fungi therefore have potential roles in the marine carbon cycle that are poorly understood. The absence of fungi within a general view of the structure and function of the marine carbon cycle, including a lack of mechanistic understanding of saprotroph functional biology and ecology, represent major knowledge gaps in our understanding of marine ecosystems that must be addressed. For a recent review on aquatic fungi, including marine, see: Grossart H-P, Van den Wyngaert S, Kagami M, Wurzbacher C, Cunliffe M & Rojas-Jimenez K (2019) Fungi in aquatic ecosystems. Nature Reviews Microbiology 17: 339–354.

Overall objectives: MYCO-CARB is addressing the above knowledge gaps through an innovative programme of research. Research cruises at established marine observatories are making an unprecedented assessment of active mycoplankton diversity and abundance across a range of ecosystems; from surface coastal waters to the deep open ocean. Innovative approaches, including molecular ecology tools and modelling, are establishing the impact of fungal saprotrophs on the marine carbon cycle. A culture collection of marine saprotrophic fungi is being developed, informed by the field-based surveys of natural assemblages to produce ecologically-relevant model fungi. Complementary culture-dependent and -independent systems biology methodologies will determine the underpinning biological machinery of saprotrophic marine mycoplankton. Through the MYCO-CARB research programme, we will open the marine fungal ‘black box’, revealing marine mycoplankton functional biology and ecology, and establishing their roles in the marine carbon cycle.

To study marine mycoplankton, a research cruise was undertaken in the North East Atlantic (2019) and several in the Western English Channel (2019). Because of the COVID-19 pandemic, succeeding research cruises planned for 2020 in the North East Atlantic and in the Western English Channel were cancelled and therefore limited the scope of marine ecosystem sampling. From the samples that have been collected, molecular assessments of mycoplankton communities have been made, as well as quantification of fungal biomass. Combined with associated metadata (temperature, salinity, etc.), these molecular ecology samples are being processed and will form the basis of a research publication(s) developed in 2021. Supplementary samples have been acquired from collaborators to help mitigate the impacts of the COVID-19 pandemic on the project. These additional samples are being assessed for suitability for the project.

Marine mycoplankton are likely functionally analogous to their terrestrial counterparts, including performing saprotrophy and degrading particulate organic carbon (POC) using carbohydrate-active enzymes (CAZymes). We have investigated the prevalence of transcribed oceanic fungal CAZyme genes using the freely available Marine Atlas of Tara Ocean Unigenes database. We revealed an abundance of unique transcribed fungal glycoside hydrolases in the open ocean, including a particularly high number that act upon cellulose in surface waters and the deep chlorophyll maximum (DCM). A variety of other glycoside hydrolases acting on a range of biogeochemically important POC-associated polysaccharides including β-glucans and chitin were also found. This analysis demonstrates that mycoplankton are active saprotrophs in the open ocean and paves the way for future research into the depth-dependent roles of marine fungi in oceanic POC cycling, including the biological carbon pump. This work has been recently published: Chrismas N & M Cunliffe (2020) Depth-dependent mycoplankton glycoside hydrolase gene activity in the open ocean - evidence from the Tara Oceans eukaryote metatranscriptomes. The ISME Journal 14: 2361–2365.

A culture collection of marine saprotrophic fungi has been established using samples collected from a range of marine ecosystems, including the North East Atlantic and the Western English Channel. To date, there are 323 strains that are spread across 3 phyla and 46 genera. The strains in the collection are in the final stages of identification and preliminary characterization (e.g. substrate range). Selected strains from the collection will be studied in detail over the remaining phase of the MYCO-CARB project.
Using available model saprotrophic fungi, preliminary assessments have been made of the biology underpinning saprotrophic capabilities. This pilot work has demonstrated the molecular basis (i.e. genes and enzymes) of how fungi degrade POC, and how fungi physically interact with POC.

The impacts of fungi-POC interaction on the wider microbial community have also been determined. Although POC is readily used by aquatic fungi and bacteria, there is a limited understanding of POC-associated interactions between these taxa. Using an available model chitin-degrading fungus and chitin microbeads, we assessed the impacts of fungi on POC-associated bacteria. We show that the presence of chytrids on POC alters concomitant bacterial community diversity and structure. We propose that fungi can act as aquatic ecosystem facilitators through saprotrophic feeding by producing ‘public goods’ from POC degradation that modify bacterial POC communities. This study suggests that fungi have complex ecological roles in aquatic POC degradation not previously considered, including the regulation of bacterial colonization, community succession and subsequent biogeochemical potential. This work has been recently published: Roberts C, Allen A, Bird K & M Cunliffe (2020) Chytrid fungi shape bacterial communities on model particulate organic matter. Biology Letters 16: 20200368.

The MYCO-CARB research programme is driven by the need to understand the biological and ecological mechanistic roles that saprotrophic mycoplankton have in the structure and function of the marine pelagic carbon cycle. A base-line understanding of mycoplankton diversity has been established in coastal waters, shelf seas and the open ocean. However, the functional roles that fungi fulfil within pelagic marine ecosystems still remain largely speculative. Functional roles must be fully characterised and their underpinning biological mechanisms understood. If we consider the well-established significance of functionally analogous fungal saprotrophs in terrestrial ecosystems, then MYCO-CARB will deliver a ground-breaking paradigm shift by determining the functional biology and ecology of a currently un-characterised and enigmatic marine plankton group.

Progress so far beyond the state of the art has been partially addressed for following key question:

What are the underpinning biological mechanisms that define and determine the functional roles that saprotrophic fungi have in the marine carbon cycle?
As outlined in the previous section, the prevalence of transcribed fungal CAZyme genes was determined using the freely available Marine Atlas of Tara Ocean Unigenes database. Active transcribed fungal glycoside hydrolases are in the open ocean, including a particularly high number that act upon cellulose in surface waters and the deep chlorophyll maximum (DCM). A variety of other glycoside hydrolases acting on a range of important POC-associated polysaccharides including β-glucans and chitin are also active. Chrismas N & M Cunliffe (2020) Depth-dependent mycoplankton glycoside hydrolase gene activity in the open ocean - evidence from the Tara Oceans eukaryote metatranscriptomes. The ISME Journal 14: 2361–2365.

Other expected results from MYCO-CARB will also address the following overarching key questions:

How do saprotrophic mycoplankton interact with bacterioplankton?

What is the structure of the active marine ‘mycobiome’?

What is the nature and magnitude of the roles of fungal saprotrophs in the marine carbon cycle, and does their impact vary between ecosystems and key ecological processes?

Through the MYCO-CARB research programme, we will open the marine fungal ‘black box’ and shed light on a currently enigmatic and understudied plankton group. MYCO-CARB will reveal marine mycoplankton functional biology and ecology, and establish the roles of saprotrophic fungi in the marine carbon cycle.

A selection of cultures from the MYCO-CARB marine fungi culture collection

FUNCTIONAL BIOLOGY AND ECOLOGY OF PLANKTONIC MARINE FUNGI – Revealing the mechanistic basis of the roles of mycoplankton in the marine carbon cycle

Periodic Reporting for period 3 - MYCO-CARB (FUNCTIONAL BIOLOGY AND ECOLOGY OF PLANKTONIC MARINE FUNGI – Revealing the mechanistic basis of the roles of mycoplankton in the marine carbon cycle)

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