Seasonal Dynamics of Pelagic Mycoplanktonic Communities: Interplay of Taxon Abundance, Temporal Occurrence, and Biotic Interactions.

Stefanos Banos,Tim Richter-Heitmann,Gunnar Gerdts,Karen H Wiltshire,Marlis Reich,Antje Wichels,Maarten Boersma,Deisy Morselli Gysi,Frank Oliver Glöckner

doi:10.3389/fmicb.2020.01305

Abstract

Marine fungi are an important component of pelagic planktonic communities. However, it is not yet clear how individual fungal taxa are integrated in marine processes of the microbial loop and food webs. Most likely, biotic interactions play a major role in shaping the fungal community structure. Thus, the aim of our work was to identify possible biotic interactions of mycoplankton with phytoplankton and zooplankton groups and among fungi, and to investigate whether there is coherence between interactions and the dynamics, abundance and temporal occurrence of individual fungal OTUs. Marine surface water was sampled weekly over the course of 1 year, in the vicinity of the island of Helgoland in the German Bight (North Sea). The mycoplankton community was analyzed using 18S rRNA gene tag-sequencing and the identified dynamics were correlated to environmental data including phytoplankton, zooplankton, and abiotic factors. Finally, co-occurrence patterns of fungal taxa were detected with network analyses based on weighted topological overlaps (wTO). Of all abundant and persistent OTUs, 77% showed no biotic relations suggesting a saprotrophic lifestyle. Of all other fungal OTUs, nearly the half (44%) had at least one significant negative relationship, especially with zooplankton and other fungi, or to a lesser extent with phytoplankton. These findings suggest that mycoplankton OTUs are embedded into marine food web chains via highly complex and manifold relationships such as parasitism, predation, grazing, or allelopathy. Furthermore, about one third of all rare OTUs were part of a dense fungal co-occurrence network probably stabilizing the fungal community against environmental changes and acting as functional guilds or being involved in fungal cross-feeding. Placed in an ecological context, strong antagonistic relationships of the mycoplankton community with other components of the plankton suggest that: (i) there is a top-down control by fungi on zooplankton and phytoplankton; (ii) fungi serve as a food source for zooplankton and thereby transfer nutrients and organic material; (iii) the dynamics of fungi harmful to other plankton groups are controlled by antagonistic fungal taxa.

Highlights

The marine biological pump plays a central role in Earth’s ecosystems
We investigated the patterns of the abundant fungal OTU dynamics in more detail, as they are the product of the interplay of the taxon’s life style and the relationship with environmental factors
Given (i) that the mycoplankton community was dominated by diverse phyla during the sampling period, (ii) that within the fungal OTU dynamics the increase/decrease of the sequence reads was sequential, (iii) that the patterns have been divided into only four categories due to similar temporal succession curves, and (iv) that these resemble already published patterns of aquatic microbes (Gerphagnon et al, 2013; Needham et al, 2013), we suppose that the majority of the sequence data is derived from taxa that actively respond to their environment

Summary

Introduction

The marine biological pump plays a central role in Earth’s ecosystems. The core of this biological pump is the carbon cycle. In this process, carbon is drawn down from the atmosphere into the ocean by phytoplankton-driven photosynthesis. The generated organic carbon is largely degraded and taken up by microorganisms and subsequently transferred to the ocean’s depths or to higher trophic levels via the food web (Turner, 2015). Marine fungi are still largely excluded, despite the increasing evidence that they can assimilate and decompose essential amounts of phytoplankton-derived organic matter (Gutierrez et al, 2011; Cunliffe et al, 2017), influence phytoplankton population dynamics (Gutierrez et al, 2016), or may act as trophic link between phytoplankton and zooplankton via a marine mycoloop (Amend et al, 2019) analogous to the one described for freshwater systems (Kagami et al, 2014)

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