A 17-year time-series of fungal environmental DNA from a coastal marine ecosystem reveals long-term seasonal-scale and inter-annual diversity patterns

Abstract

Changing patterns in diversity are a feature of many habitats, with seasonality a major driver of ecosystem structure and function. In coastal marine plankton-based ecosystems, seasonality has been established through long-term time-series of bacterioplankton and protists. Alongside these groups, fungi also inhabit coastal marine ecosystems. If and how marine fungi show long-term intra- and inter-annual diversity patterns is unknown, preventing a comprehensive understanding of marine fungal ecology. Here, we use a 17-year environmental DNA time-series from the English Channel to determine long-term marine fungal diversity patterns. We show that fungal community structure progresses at seasonal and monthly scales and is only weakly related to environmental parameters. Communities restructured every 52-weeks suggesting long-term stability in diversity patterns. Some major marine fungal genera have clear inter-annual recurrence patterns, re-appearing in the annual cycle at the same period. Low relative abundance taxa that are likely non-marine show seasonal input to the coastal marine ecosystem suggesting land–sea exchange regularly takes place. Our results demonstrate long-term intra- and inter-annual marine fungal diversity patterns. We anticipate this study could form the basis for better understanding the ecology of marine fungi and how they fit in the structure and function of the wider coastal marine ecosystem.

Planktonic Marine Fungi: A Review

“…Coastal planktonic fungi typically constitute a mixture of marine and terrestrial lineages (Chrismas et al., 2023). There are currently 1,898 described species of marine fungi (https://www.marinefungi.org/, 12 September 2023; Calabon et al., 2023), but their actual diversity is estimated to be much higher, with some studies stating that only around 1% of marine fungi have been identified (Gladfelter et al., 2019; Jones, 2011).…”

Physiological and morphological plasticity in response to nitrogen availability of a yeast widely distributed in the open ocean

“…In addition to saprotrophy, marine yeasts are associated with other trophic interactions, including predation by zooplankton (Cleary et al 2016 ), and parasitism of phytoplankton (Li et al 2016 ) and zooplankton (Seki and Fulton 1969 ). Marine yeast abundances have been shown to fluctuate by several orders of magnitude over relatively short time-scales during a spring phytoplankton bloom (Priest et al 2021 ), while interannual recurrence patterns of yeast-containing taxa further suggest a dynamic role for yeasts in marine plankton communities (Taylor and Cunliffe 2016 , Chrismas et al 2023 ). Absolute abundances of marine yeast taxa have been significantly positively correlated with environmental concentrations of nitrogen-containing compounds (Taylor and Cunliffe 2016 , Priest et al 2021 ), but quantitative data describing marine yeast responses to nitrogen availability are currently lacking in contrast with other major plankton groups.…”

Marine Fungal Diversity and Dynamics in the Gulf of Trieste (Northern Adriatic Sea)

“…One of the main limiting factors for DNA-based assessment of mycoplankton is the bias from "generic" eukaryotic primers (targeting the 18S rRNA gene [ 13 ]), which can lead to a lack of amplified fragments and consequently an underestimation of the proportion and diversity of fungi in biological communities [ 9 , 14 ]. Therefore, the use of fungal-specific barcodes, such as those targeting the ribosomal nuclear gene internal transcribed spacer (ITS) [ 15 ] or the 18S rRNA gene [ 16 ], can provide greater insight into marine fungi biodiversity, although requiring ad hoc amplification, sequencing, and data analysis. In addition, mycoplankton can have patchy and highly variable spatiotemporal distribution patterns compared to bacterioplankton [ 9 , 15 , 17 ], making data analysis and interpretation more complex.…”

“…Therefore, the use of fungal-specific barcodes, such as those targeting the ribosomal nuclear gene internal transcribed spacer (ITS) [ 15 ] or the 18S rRNA gene [ 16 ], can provide greater insight into marine fungi biodiversity, although requiring ad hoc amplification, sequencing, and data analysis. In addition, mycoplankton can have patchy and highly variable spatiotemporal distribution patterns compared to bacterioplankton [ 9 , 15 , 17 ], making data analysis and interpretation more complex. Therefore, additional efforts are needed to explore the diversity and ecological role of fungi in marine habitats.…”

“…Here, we provide new insights into fungal communities in coastal environments, where mycoplankton are thought to play a particularly important role in organic matter cycling [ 4 ]. In this perspective, Long Term Ecological Research (LTER) stations represent a valuable resource and strategic advantage to assess patterns of mycoplankton diversity [ 15 ]. At the LTER C1 station (Gulf of Trieste, northern Adriatic Sea), seawater was sampled monthly over 1.5 years, and DNA metabarcoding targeting the ITS1 region was used to investigate mycoplankton composition, distribution, and key environmental factors influencing their temporal patterns, an effort directed to expand current knowledge of the structure and dynamics of coastal marine mycobiome.…”