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

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.

Fungal endophytes vary by species, tissue type, and life cycle stage in intertidal macroalgae.

Fungal symbionts of terrestrial plants are among the most widespread and well-studied symbioses, relatively little is known about fungi that are associated with macroalgae. To fill the gap in marine fungal taxonomy, we combined simple culture methods with amplicon sequencing to characterize the fungal communities associated with three brown (Sargassum muticum, Pelvetia canaliculata, and Himanthalia elongata) and two red (Mastocarpus stellatus and Chondrus crispus) macroalgae from one intertidal zone. In addition to characterizing novel fungal diversity, we tested three hypotheses: fungal diversity and community composition vary (i) among species distributed at different tidal heights, (ii) among tissue types (apices, mid-thallus, and stipe), and (iii) among "isomorphic" C. crispus life cycle stages. Almost 70% of our reads were classified as Ascomycota, 29% as Basidiomycota, and 1% that could not be classified to a phylum. Thirty fungal isolates were obtained, 18 of which were also detected with amplicon sequencing. Fungal communities differed by host and tissue type. Interestingly, P. canaliculata, a fucoid at the extreme high intertidal, did not show differences in fungal diversity across the thallus. As found in filamentous algal endophytes, fungal diversity varied among the three life cycle stages in C. crispus. Female gametophytes were also compositionally more dispersed as compared to the fewer variable tetrasporophytes and male gametophytes. We demonstrate the utility of combining relatively simple cultivation and sequencing approaches to characterize and study macroalgal-fungal associations and highlight the need to understand the role of fungi in near-shore marine ecosystems.

Macromolecular composition and substrate range of three marine fungi across major cell types.

Marine fungi exist as three major cell types: unicellular yeasts, filamentous hyphae and zoosporic early-diverging forms, such as the Chytridiomycota (chytrids). To begin to understand the ecological and biogeochemical influence of these cell types within the wider context of other plankton groups, cell size and macromolecular composition must be assessed across all three cell types. Using a mass-balance approach to culture, we describe quantitative differences in substrate uptake and subsequent macromolecular distribution in three model marine fungi: the yeast Metschnikowia zobellii, the filamentous Epicoccum nigrum and chytrid Rhizophydium littoreum. We compared these model cell types with select oleaginous phytoplankton of specific biotechnological interest through metanalysis. We hypothesise that fungal cell types will maintain a significantly different macromolecular composition to one another and further represent an alternative grazing material to bacterioplankton and phytoplankton for higher trophic levels. Assessment of carbon substrate range and utilisation using phenotype arrays suggests that marine fungi have a wide substrate range. Fungi also process organic matter to an elevated-lipid macromolecular composition with reduced-protein content. Because of their size and increased lipid composition compared to other plankton groups, we propose that fungi represent a compositionally distinct, energy-rich grazing resource in marine ecosystems. We propose that marine fungi could act as vectors of organic matter transfer across trophic boundaries, and supplement our existing understanding of the microbial loop and carbon transfer in marine ecosystems.

Feedback mechanisms stabilise degraded turf algal systems at a CO2 seep site.

Human activities are rapidly changing the structure and function of coastal marine ecosystems. Large-scale replacement of kelp forests and coral reefs with turf algal mats is resulting in homogenous habitats that have less ecological and human value. Ocean acidification has strong potential to substantially favour turf algae growth, which led us to examine the mechanisms that stabilise turf algal states. Here we show that ocean acidification promotes turf algae over corals and macroalgae, mediating new habitat conditions that create stabilising feedback loops (altered physicochemical environment and microbial community, and an inhibition of recruitment) capable of locking turf systems in place. Such feedbacks help explain why degraded coastal habitats persist after being initially pushed past the tipping point by global and local anthropogenic stressors. An understanding of the mechanisms that stabilise degraded coastal habitats can be incorporated into adaptive management to better protect the contribution of coastal systems to human wellbeing.

Homogeneous environmental selection dominates microbial community assembly in the oligotrophic South Pacific Gyre.

Oligotrophic subtropical gyres are the largest continuous biomes on Earth and play a key role in global biogeochemical cycles. Microbial communities govern primary production and carbon cycling in the oligotrophic South Pacific Gyre, yet the ecological processes which underpin microbial biogeography in the region remain understudied. We investigated microbial biogeography and community assembly processes at three depths over a ~2,000-km the transect was longitudinal, so ran from 32°S, 170°W to 32°S, 152°W). Thus the latitude (32°S) was constant. Microbial communities in the surface waters (15 and 50 m) were remarkably similar across the transect, whilst communities at the deep chlorophyll maximum were distinct from the surface waters and displayed greater compositional heterogeneity. An ecological null model approach indicated that homogeneous selection was the dominant community assembly process in both the surface waters (100%) and at the deep chlorophyll maximum (91.81%), although variable selection (2.34%) and stochastic processes (5.85%) had a minor influence at the deep chlorophyll maximum. Homogeneous selection (76.69%77.90%), dispersal limitation (15.00%-20.05%) and variable selection (3.01%-7.11%) influenced community assembly between the surface waters and the deep chlorophyll maximum. Seawater density and temperature, which were correlated, were the most important environmental modulators of the balance between stochastic and deterministic assembly processes. Our findings demonstrate remarkable similarity in microbial community composition across longitudinal scales in the oligotrophic South Pacific Gyre, underpinned by strong environmental selection which overwhelms the influence of ecological drift. These data significantly advance our understanding of microbial community dynamics in the oligotrophic subtropical gyres which dominate the Earth's surface.

Chytrid fungi shape bacterial communities on model particulate organic matter.

Microbial colonization and degradation of particulate organic matter (POM) are important processes that influence the structure and function of aquatic ecosystems. Although POM is readily used by aquatic fungi and bacteria, there is a limited understanding of POM-associated interactions between these taxa, particularly for early-diverging fungal lineages. Using a model ecological system with the chitin-degrading freshwater chytrid fungus Rhizoclosmatium globosum and chitin microbeads, we assessed the impacts of chytrid fungi on POM-associated bacteria. We show that the presence of chytrids on POM alters concomitant bacterial community diversity and structure, including differing responses between chytrid life stages. We propose that chytrids can act as ecosystem facilitators through saprotrophic feeding by producing 'public goods' from POM degradation that modify bacterial POM communities. This study suggests that chytrid fungi have complex ecological roles in aquatic POM degradation not previously considered, including the regulation of bacterial colonization, community succession and subsequent biogeochemical potential.

Subtle bacterioplankton community responses to elevated CO2 and warming in the oligotrophic South Pacific gyre.

Bacterioplankton play a critical role in primary production, carbon cycling, and nutrient cycling in the oligotrophic ocean. To investigate the effect of elevated CO2 and warming on the composition and function of bacterioplankton communities in oligotrophic waters, we performed two trace-metal clean deck board incubation experiments during the New Zealand GEOTRACES transect of the South Pacific gyre (SPG). High-throughput amplicon sequencing of the 16S rRNA gene revealed that bacterioplankton community composition was distinct between the fringe and ultra-oligotrophic centre of the SPG and changed consistently in response to elevated CO2 at the ultra-oligotrophic centre but not at the mesotrophic fringe of the SPG. The combined effects of elevated CO2 and warming resulted in a high degree of heterogeneity between replicate communities. Community-level protein synthesis rates (3 H-Leucine incorporation) and bacterioplankton abundance were not affected by elevated CO2 alone or in combination with warming at the fringe or ultra-oligotrophic centre of the SPG. These data suggest bacterioplankton community responses to elevated CO2 may be modulated by nutrient regimes in open ocean ecosystems and highlight the need for further investigation in expanding oligotrophic subtropical gyres.

Tropical CO2 seeps reveal the impact of ocean acidification on coral reef invertebrate recruitment.

Rising atmospheric CO2 concentrations are causing ocean acidification by reducing seawater pH and carbonate saturation levels. Laboratory studies have demonstrated that many larval and juvenile marine invertebrates are vulnerable to these changes in surface ocean chemistry, but challenges remain in predicting effects at community and ecosystem levels. We investigated the effect of ocean acidification on invertebrate recruitment at two coral reef CO2 seeps in Papua New Guinea. Invertebrate communities differed significantly between 'reference' (median pH7.97, 8.00), 'high CO2' (median pH7.77, 7.79), and 'extreme CO2' (median pH7.32, 7.68) conditions at each reef. There were also significant reductions in calcifying taxa, copepods and amphipods as CO2 levels increased. The observed shifts in recruitment were comparable to those previously described in the Mediterranean, revealing an ecological mechanism by which shallow coastal systems are affected by near-future levels of ocean acidification.