Ruth Louise Airs

Ubiquitous marine microalgae and bacteria produce the abundant organosulfur compound dimethylsulfoniopropionate (DMSP) and/or catabolize it to climate-active gases, such as dimethylsulfide (DMS), with major consequences for global biogeochemistry and climate. However, their relative and dynamic roles in DMSP synthesis and catabolism remain poorly resolved, particularly during natural bloom events. Here, we combined metagenomics and metatranscriptomics, with measurements of intracellular/particulate DMSP (DMSPp), DMS concentrations, and DMSPp production rates, as well as microscopy and flow cytometry, to predict the key microbes and enzymes driving DMSP/DMS dynamics during a spring–summer bloom in the Western English Channel. Microalgae and bacteria expressing the DMSP synthesis genes DSYB/DSYE and dsyB were likely major and significant DMSP producers, respectively, except during the largest observed DMSP spike. This spike coincided with elevated Synechococcus and autotrophic flagellate biomass but minimal DMSP synthesis gene expression. Axenic Synechococcus strains contained no detectable DMSP, implying that flagellates with novel DMSP synthesis genes were likely responsible. Microbial DMSP import potential far exceeded catabolism, suggesting strong selection for DMSP uptake. Bacteria were the major predicted DMSP degraders, with DMSP demethylation potential dwarfing cleavage. However, the highest DMS concentrations were linked to Haptophyta expressing the DMSP lyase gene Alma, implying the significance of algal DMSP cleavage. Methanethiol-dependent DMS production was also likely important, with bacterial mddH transcripts coinciding with another major DMS spike. Overall, these results imply dynamic and contrasting roles of microalgae and bacteria, and their pathways, in coastal DMSP/DMS and sulfur cycling.

Glycine betaine (GBT) is a nitrogenous osmolyte ubiquitous throughout the marine environment. Despite its widespread occurrence and significance in microbial cycling, knowledge of the seasonality of this compound is lacking. Here, we present a seasonal dataset of GBT concentrations in marine suspended particulate material. Analysing coastal waters in the Western English Channel, GBT peaked in summer and autumn but did not follow the observed maxima in total phytoplankton biomass or chlorophyll a. Instead, we found evidence that GBT concentrations were associated with specific phytoplankton groups or species, particularly in the summer when GBT correlated with dinoflagellate biomass. In contrast, autumn maxima corresponded with a period of rapidly changing salinity and nutrient availability, with potential contributions from some phytoplankton species and Harpacticoid copepods. This suggests distinct environmental drivers for different periods of the GBT seasonality. Building on evidence that GBT and dinoflagellate biomass peak in summer, concomitantly with low nutrients, we propose that GBT positively affects dinoflagellate fitness, allowing them to outcompete other plankton when inorganic nutrients are depleted. By using this assumption, we improved the performance of a marine ecosystem model to reproduce the observed increase in dinoflagellates biomass in the transition from spring to summer. This work sheds light on the interplay between phytoplankton succession, competitive advantage and changing environmental factors relevant to climate change. It paves the way for future multidisciplinary research aiming to understand the importance of dinoflagellates in key coastal ecosystems and their potential significance for methylamine production, compounds relevant for particle growth in atmospheric chemistry.

Choline and glycine betaine (GBT) are utilized as osmolytes to counteract osmotic stress, but also constitute important nutrient sources for many marine microbes. Bacterial catabolism of these substrates can then lead to the production of climate active trace gases such as methylamine and methane. Using radiotracers, we investigated prokaryotic choline/GBT uptake and determined biotic and abiotic factors driving these processes in the Western English Channel, UK. Kinetic uptake parameters indicated high affinity (nM range) for both osmolytes and showed a seasonal pattern for choline uptake. Generalized linear modeling of uptake parameters suggested a significant influence of sea surface temperature and salinity on prokaryotic uptake of both osmolytes. The presence of diatoms significantly influenced prokaryotic choline/GBT uptake dynamics. Choline uptake was further related to the occurrence of Phaeocystis spp., which were highly abundant in the phytoplankton community during spring, and dinoflagellates abundance during summer. While Rhodobacteraceae were the most important bacterial drivers for prokaryotic choline uptake, prokaryotic GBT uptake was associated with various groups such as SAR11 (Pelagibacterales) and Gammaproteobacteria, suggesting a wider capacity for GBT catabolism than previously recognized. Furthermore, using a newly developed approach we determined the first available data for dissolved GBT concentrations in seawater and found both osmolytes to be at the sub‐nanomolar range. Together, this study improves our understanding of the biogeochemical cycling of these environmentally important osmolytes and highlights how their cycles may be affected by a changing climate.

The Southern Ocean is a critical component of Earth’s climate system, but its remoteness makes it challenging to develop a holistic understanding of its processes from the small to the large scale. As a result, our knowledge of this vast region remains largely incomplete. The Antarctic Circumnavigation Expedition (ACE, austral summer 2016/2017) surveyed a large number of variables describing the dynamic state of the ocean and the atmosphere, the freshwater cycle, atmospheric chemistry, ocean biogeochemistry and microbiology. This circumpolar cruise included visits to twelve remote islands, the marginal ice zone, and the Antarctic coast. Here, we use 111 of the observed variables to study the latitudinal gradients, seasonality, shorter term variations, the geographic setting of environmental processes, and interactions between them over the duration of 90 days. To reduce the dimensionality and complexity of the dataset and make the relations between variables interpretable, we applied a sparse Principal Component Analysis (sPCA), which describes environmental processes through 14 latent variables. To derive a robust statistical perspective on these processes and to estimate the uncertainty in the sPCA decomposition, we have developed a bootstrap approach. We identified temporal patterns from diurnal to seasonal cycles, as well as geographical gradients and “hotspots” of interaction. Our results establish connections of oceanic, atmospheric, biological and terrestrial processes in an innovative way, while confirming many well known relations of the Southern Ocean system. More specifically, we identify: the important role of the oceanic circulations, frontal zones, and islands in shaping the nutrient availability that controls biological community composition and productivity; that sea ice predominantly controls sea water salinity, dampens the wave field, and is associated with increased phytoplankton growth and net community productivity possibly due to iron fertilization and reduced light limitation; and clear regional patterns of aerosol characteristics emerged, stressing the role of the sea state, atmospheric chemical processing, as well as source processes near “hotspots” for the availability of cloud condensation nuclei and hence cloud formation. A set of key variables and their combinations, such as the difference between the air and sea surface temperature, atmospheric pressure, sea surface height, geostrophic currents, upper ocean layer light intensity, surface wind speed and relative humidity, played an important role in the majority of latent variables, highlighting their importance for a large variety of processes and the necessity for Earth System Models to represent them adequately. In conclusion, our study highlights the use of sPCA to identify key ocean-atmosphere interactions across physical, chemical, and biological processes and their associated spatio-temporal scales. The sPCA processing code is available as open-access and we believe that our approach is widely applicable to other environmental field studies.

Seaweeds contain many varied and commercially valuable components, from individual pigments and metabolites through to whole biomass, and yet they remain an under cultivated and underutilised commodity. Currently, commercial exploitation of seaweeds is predominantly limited to whole biomass consumption or single product extracts for the food industry. The development of a seaweed biorefinery, based around multiple products and services, could provide an important opportunity to exploit new and currently underexplored markets. Here, we assessed the native and invasive seaweeds on the South West coast of the UK to determine their characteristics and potential for exploitation through a biorefinery pipeline, looking at multiple components including pigments, carbohydrates, lipids, proteins and other metabolites.

Macroalgae drive the largest CO₂ flux fixed globally by marine macrophytes. Most of the resulting biomass is exported through the coastal ocean as detritus and yet almost no field measurements have verified its potential net sequestration in marine sediments. This gap limits the scope for the inclusion of macroalgae within blue carbon schemes that support ocean carbon sequestration globally, and the understanding of the role their carbon plays within distal food webs. Here, we pursued three lines of evidence (eDNA sequencing, Bayesian Stable Isotope Mixing Modeling, and benthic‐pelagic process measurements) to generate needed, novel data addressing this gap. To this end, a 13‐month study was undertaken at a deep coastal sedimentary site in the English Channel, and the surrounding shoreline of Plymouth, UK. The eDNA sequencing indicated that detritus from most macroalgae in surrounding shores occurs within deep, coastal sediments, with detritus supply reflecting the seasonal ecology of individual species. Bayesian stable isotope mixing modeling [C and N] highlighted its vital role in supporting the deep coastal benthic food web (22–36% of diets), especially when other resources are seasonally low. The magnitude of detritus uptake within the food web and sediments varies seasonally, with an average net sedimentary organic macroalgal carbon sequestration of 8.75 g C·m⁻²·yr⁻¹. The average net sequestration of particulate organic carbon in sediments is 58.74 g C·m⁻²·yr⁻¹, the two rates corresponding to 4–5% and 26–37% of those associated with mangroves, salt marshes, and seagrass beds, systems more readily identified as blue carbon habitats. These novel data provide important first estimates that help to contextualize the importance of macroalgal‐sedimentary connectivity for deep coastal food webs, and measured fluxes help constrain its role within global blue carbon that can support policy development. At a time when climate change mitigation is at the foreground of environmental policy development, embracing the full potential of the ocean in supporting climate regulation via CO₂ sequestration is a necessity.

Coastal saltmarsh sediments represent an important source of natural methane emissions, much of which originates from quaternary and methylated amines, such as choline and trimethylamine. In this study, we combine DNA stable isotope probing with high throughput sequencing of 16S rRNA genes and ¹³C₂-choline enriched metagenomes, followed by metagenome data assembly, to identify the key microbes responsible for methanogenesis from choline. Microcosm incubation with ¹³C₂-choline leads to the formation of trimethylamine and subsequent methane production, suggesting that choline-dependent methanogenesis is a two-step process involving trimethylamine as the key intermediate. Amplicon sequencing analysis identifies Deltaproteobacteria of the genera Pelobacter as the major choline utilizers. Methanogenic Archaea of the genera Methanococcoides become enriched in choline-amended microcosms, indicating their role in methane formation from trimethylamine. The binning of metagenomic DNA results in the identification of bins classified as Pelobacter and Methanococcoides. Analyses of these bins reveal that Pelobacter have the genetic potential to degrade choline to trimethylamine using the choline-trimethylamine lyase pathway, whereas Methanococcoides are capable of methanogenesis using the pyrrolysine-containing trimethylamine methyltransferase pathway. Together, our data provide a new insight on the diversity of choline utilizing organisms in coastal sediments and support a syntrophic relationship between Bacteria and Archaea as the dominant route for methanogenesis from choline in this environment.