Algal holobionts: challenges and opportunities

In the dilute planktonic ocean, point source release of dissolved organic matter (DOM) from individual microalgal cells, either through slow exudation or sudden lysis, generates nutrient rich microenvironments which heterotrophic bacteria may exploit through chemotaxis. The chemically-mediated interactions between microalgae and bacteria played out within these microenvironments are predicted to have profound impacts on microbial growth and chemical cycling in the pelagic ocean. However, these interactions have never been studied in situ because of technological limitations, restricting our capacity to decipher the microscale relationships between marine microbes in the environment. Here Dr Raina will describe the application of a purpose-designed microfluidic chip, the In Situ Chemotaxis Assay (ISCA), to assess the ability of marine microbes to respond to microscale chemical cues in their natural environment. When deployed in the ocean, the ISCA generates diffusing microplumes of microalgae-derived DOM, and trap motile microbes attracted to these chemicals. Flow-cytometry and metagenomic analyses subsequently determine the strength of chemotaxis and reveal the identity and metabolic capabilities of the responding microbes. Dr Raina and his team used the ISCA to investigate the response of marine microbes to microscale patches of DOM derived from globally distributed and diverse microalgal species. He observed specific microalgae-bacteria associations underpinned by chemotactic behaviours, as well as the identity of important microalgae-derived chemical cues that attract these specific bacteria. By unveiling a rich tapestry of microbial interactions through in situ microscale observations, Dr Raina’s results provide the basis for quantifying the role of chemotaxis in accessing microscale hotspots in marine systems, and an opportunity to scale up the impact of these processes on the ocean’s biogeochemistry.

Seaweeds underpin some of the most extensive and productive coastal ecosystems globally. However, health and fitness of seaweeds can be impacted through surface microbial colonisation consisting mainly of bacteria. Just like land plants, seaweeds employ a range of anti and pro-microbials to deter, reduce or ‘garden’ epibacterial colonisation. Like plants, seaweeds are known to be prolific producers of BVOCs (biogenic volatile organic compounds) in the marine environment. However, unlike plants the ecological roles of seaweed BVOCs, particularly in mediating host-microbe interactions, are poorly explored when compared to the role of non-volatile compounds. Although BVOC production is known to vary temporally and with abiotic factors in seaweeds, unlike land plants we do not know yet how such variations may alter ecological interactions of seaweeds with microbes. In this talk, Dr Saha will discuss how such BVOC mediated interaction may vary with abiotic stressors. Despite being a diverse source of antimicrobial compounds seaweeds have not been evaluated for their chemical defence mechanism to remove microbiological contamination by human and environmental pathogens and thus improve water quality. Thus, ability of these macrophytes to reduce microbiological contamination is not known in the UK and surrounding waters. In this talk we will also discuss the potential of seaweeds to reduce human pathogen load in the water column to improve water quality.

Collectively, algae account for nearly half of Earth’s primary production; increasingly, their interactions with parasites are recognised as a key to the dynamics of microbial pelagic food webs. In temperate and cold coastal areas, macroalgae are ecosystem engineers and provide habitat for fish and other animals. Fuelled by soaring demand, the current growth of algal cultivation sits in the wider context of intensifying use and increasing dependency of mankind on the oceans. On land, domestication of plants has fundamentally transformed human societies and terrestrial ecosystems. Since the Neolithic, agriculture has shaped landscapes, cultures, societal values, and governance, including our trade rules and conservation policies. The health of plants dictates agricultural yields as well as ecosystem health: pathogens co-evolve with domesticated species, whilst intensification of production favours outbreaks as well as the emergence of novel pathogens. In marine coastal areas, algal aquaculture represents a comparable mutation, that only occurs at a vastly higher pace than agriculture spread historically. This biological pressure is compounded by a faster rate of climate change compared to terrestrial systems. Alarmingly, reports of diseased or declining wild macroalgal populations, as well as significant losses in seaweed farms accumulate worldwide. In this talk, Dr Gachon will brush upon the work performed in her group that seeks to lay a basis towards tackling these questions.

In the marine environment, macroalgae have established an intimate connection with associated microbial communities (bacteria, fungi, diatoms), and altogether they constitute the algal holobiont. However, the mechanisms governing the acquisition, composition and dynamics of microbes at the algal surface are still poorly understood. Laminariales (or kelps), such as Laminaria digitata, are large brown algae, which feature a unique iodine metabolism, involved in anti-oxidative protection and chemical defenses, and which might participate in the control of microbial surface colonisation. L. digitata constitutes a model of choice to explore the functional adaptation of its associated microbiota. Using a metabarcoding approach, we have characterised the microbial communities of L. digitata sporophytes under natural conditions, by comparing the microbial taxonomic composition and structure of different surface zones. These results confirmed the importance of the environment on the acquisition of specific associated bacteria that seem to vary according to algal tissues area, physiology and chemical composition along the thallus. In parallel, biochemical studies have demonstrated the presence of halogen-related enzymes in a model marine bacterium, living in association with macroalgae, some specific of iodide oxidation or others likely involved in the recycling of toxic halogen compounds. Altogether, these results suggest a potential adaptation of some surface bacteria towards iodine-based defence metabolism, conferring selective advantage during interactions with kelps, and contribute to increase our knowledge on the mechanisms governing the functioning of kelp holobionts.

Marine brown algae are key primary producers and constitute a specific habitat strongly impacting coastal marine life. Aquaculture of algae represents a fast-growing economic sector. Worryingly, this algaculture expansion is associated with an increase in infectious diseases which may have strong economic and ecological impacts. Macroalgae also harbour microorganisms, fungi and bacteria which affect their development, fitness and defence. Indeed, the algal microbiota is the place of intense chemical communications, which finely regulates the organisation of the holobiont. In this vein, Professor Prado and her team have demonstrated that the microbiota of kelps is the seat of the production of fungal chemical mediators capable of inhibiting 1) bacterial quorum sensing, a mode of intercellular communication involved in the formation of biofilms and pathogenicity as well as the 2) infection by phycopathogens of economic interest. By using multidisciplinary approaches including chemistry of natural products, she will present new insights in the ecological roles of the algal microbiota and point out the key role of the molecular dialogue. We also demonstrate that deciphering this chemical communication is a way to identify widely diverse and original natural compounds displaying potent biological activities of interest especially in regard with agrochemical and life science uses.

Dinoflagellate microalgae of family Symbiodiniaceae are essential symbionts that critically support the coral reef ecosystems. As marine biodiversity hotspots, coral reefs are home to 25% of all known marine species. Symbiodiniaceae dinoflagellates supply essential nutrients and fixed carbon to diverse coral reef organisms that range from microbes (eg foraminiferans) to animals such as giant clams, sponges, and cnidarians (eg jellyfish, sea anemones, and corals). Breakdown of coral-dinoflagellate symbiosis under environmental stress leads to coral bleaching, coral death, and eventual collapse of the coral reef ecosystem. To understand how these microalgae evolved to become an integral member in supporting diverse marine holobionts, since 2018 Dr Chan and his team have generated genome data from 18 dinoflagellate taxa encompassing 13 species predominantly from Symbiodiniaceae. Their first coral hologenome study revealed how distinct biotic partners (ie the coral animal, the symbiotic dinoflagellate, and the other microbes) contribute to sustaining a functional coral holobiont. Their comparative analyses of whole-genome sequences revealed extensive genomic divergence even among different isolates of the same dinoflagellate species, indicating lineage-specific functional innovation and phylogenetic diversity that is hidden behind subtly different morphology. The genome analysis of a thermotolerant species further revealed how whole-genome duplication had enhanced its efficiency and resilience as a symbiont in changing environments. In this talk, Dr Chan will demonstrate how he harnessed the power of genomics to clarifying diversification of dinoflagellates to become essential symbionts that contribute to the success of diverse marine holobionts.

The haptophyte Prymnesium parvum produces prymnesin toxins targeting gill breathing organisms, and their blooms often result in large-scale fish kills with significant ecological and economic implications. P. parvum also produces the sulphurous osmolyte dimethylsulphoniopropionate (DMSP), which is the major precursor of the climate-active gas dimethylsulphide (DMS). DMSP production and its microbial cycling has important roles in stress protection, global sulphur and nutrient cycling, signalling pathways and potentially climate regulation. Building on discovery of the key gene for DMSP synthesis in P. parvum, DSYB, we conducted a molecular investigation of the seasonality and importance of P. parvum and its holobiome in DMSP cycling in Norfolk Broads, UK, brackish waters. P. parvum expressing DSYB was the major source of significant DMSP concentrations in the Broads waters that stimulated DMS production. Axenic P. parvum isolates lacked DMSP lyase activity indicating that the algal associated microbes were more likely responsible for this DMS production. Indeed, bacteria with DMSP lyases were abundant and active during and just after the P. parvum bloom but scarce under non-bloom conditions. This case study provides novel insights into the potential importance of P. parvum (and potentially other ecologically invasive haptophytes) and associated bacteria in the DMSP dynamics of shallow brackish water lake systems and in local biogenic sulphur cycling, not generally thought to be significant sources of DMSP and DMS. 

Saccharina latissima is a canopy-forming brown alga of economic and ecological in Europe. To better understand its biology and ecology, we need more data on its associated microbiota and the importance of host-microbiota inactions in this species. This talk will summarise various aspects of Dr Dittami’s recent research on the microbiome of S. latissima. The first part will give an overview of the taxonomic composition of the S. latissima microbiome, its core components, and its variability across different parts of the algae, seasons, and regions. He will also highlight characteristic microbial signatures for healthy algae vs algae in poor health and explore to what extent the microbiome is vertically transmitted versus defined by the environment. The second part will focus on co-cultures carried out in laboratory conditions to elucidate the beneficial and harmful effects of inoculation with selected S. latissima-derived microbes. While the outcomes of these experiments were highly variable, Dr Dittami observed an overall negative correlation between host growth and the detection of AI-1-type quorum-sensing (QS) compounds in the culture medium. Furthermore, he showed that the medium from algae exposed to stress can elicit the production of QS compounds in some bacteria. Together, these data contribute to our understanding of the variability of the S. latissima microbiome and establish a basis for further experimental evaluations of algal-bacterial interactions and microbiome manipulations in this system.

Seagrass meadows form highly productive ecosystems in coastal areas worldwide, where they are increasingly exposed to ocean acidification (OA). This can affect the seagrass holobiont (ie, the assemblage of the plant host and its associated epiphytic community) by changing the plant’s ecophysiology and the composition and functioning of its epiphytic community. Efficient nitrogen (N) cycling and uptake are essential to sustain plant productivity and are carried out by a variety of microbial partners as well as by the plant, from the rhizosphere to the leaves. While rhizosphere N cycling has been the focus of extensive research, precise quantification of N transformations on seagrass leaves, as well as an evaluation of the effects of ocean acidification, are missing. Here we show that complete N cycling occurs on leaves of the iconic seagrass Posidonia oceanica in the Mediterranean Sea, with OA accelerating the N cycle while the prokaryotic community structure remains largely unaffected. Ammonium uptake of the seagrass leaves was significantly increased under OA, with this need potentially sustained by increased microbial daylight N2 fixation on its leaves. Contrary to expectations, Dr Cardini and his team found higher potential nitrification rates associated with the P. oceanica phyllosphere under OA, while anoxic parts of the epiphytic biofilm were suitable microhabitats for nitrate reduction. Marine plants are bound to adapt to environmental changes if they are to persist; his work shows that functional adaptation of their N cycling microbiome plays a key role in regulating seagrass functioning in a high-CO2 world.