I am a marine microbial ecologist in the UTS Climate Change Cluster (C3) working within the Ocean Microbes Healthy Oceans research program.
My research focuses on developing new tools to quantify and visualise the interactions that take place between marine microbes at the micrometer-scale. This will lead to a better understanding of the processes that influence the productivity of the world’s oceans, as well as biogeochemical cycles and global climate.
In 2016 I was awarded an ARC DECRA which gives me the opportunity to combine new approaches in microfluidics, chemistry and oceanography to quantify carbon uptake by individual microbes in their natural environment.
I grew up in the south of France and prior to joining UTS completed my PhD in 2013 at James Cook University.
2016–2019 ARC DECRA Fellow, Ocean Microbes: Healthy Oceans research program (mentor and supervisor Assoc.Prof. Justin Seymour, UTS: Climate Change Cluster (C3))
2016 UTS Chancellor’s Postdoctoral Research Fellowship supervisor Assoc. Prof. Justin Seymour, UTS:Climate Change Cluster (C3))
2014–2015 Postdoctoral Research Associate (funded by Gordon and Betty Moore Foundation grant to JS), Ocean Microbes: Healthy Oceans research program (supervisor Assoc. Prof. Justin Seymour, UTS: Climate Change Cluster (C3))
2016 UTS Vice Chancellor’s Early Career Research Excellence Award
2016 J.G. Russell Award for most talented young researcher in the basic sciences, Australian Academy of Science
2014 Tom Brock Postdoctoral Award for the most innovative research by an early career scientist at the 15th International Symposium on Microbial Ecology (ISME) (Seoul, South Korea);
2013 Virginia Chadwick Award
2012 AIMS@JCU Annual Student Seminar Day Best Presentation Award
2010 Best Student Poster Award, 13th International Symposium on Microbial Ecology (ISME) (Seattle, USA)
2008 AIMS@JCU Annual Student Seminar Day Best Presentation Award –
PNAS; Current BIology; Nature Communications; ISME Journal;
Molecular Ecology; Scientific Reports; Global Biogeochemical Cycles; Marine Chemistry;
Coral Reefs; Marine Biology among others.
Can supervise: YES
- Marine microbial ecology
- Algal bacterial interactions
- Microbial imaging
- Coral symbiosis
Gao, C, Fernandez, VI, Lee, KS, Fenizia, S, Pohnert, G, Seymour, JR, Raina, J-B & Stocker, R 2020, 'Single-cell bacterial transcription measurements reveal the importance of dimethylsulfoniopropionate (DMSP) hotspots in ocean sulfur cycling.', Nature communications, vol. 11, no. 1, p. 1942.View/Download from: Publisher's site
Dimethylsulfoniopropionate (DMSP) is a pivotal compound in marine biogeochemical cycles and a key chemical currency in microbial interactions. Marine bacteria transform DMSP via two competing pathways with considerably different biogeochemical implications: demethylation channels sulfur into the microbial food web, whereas cleavage releases sulfur into the atmosphere. Here, we present single-cell measurements of the expression of these two pathways using engineered fluorescent reporter strains of Ruegeria pomeroyi DSS-3, and find that external DMSP concentration dictates the relative expression of the two pathways. DMSP induces an upregulation of both pathways, but only at high concentrations (>1 μM for demethylation; >35 nM for cleavage), characteristic of microscale hotspots such as the vicinity of phytoplankton cells. Co-incubations between DMSP-producing microalgae and bacteria revealed an increase in cleavage pathway expression close to the microalgae's surface. These results indicate that bacterial utilization of microscale DMSP hotspots is an important determinant of the fate of sulfur in the ocean.
Matthews, JL, Raina, J-B, Kahlke, T, Seymour, JR, van Oppen, MJH & Suggett, DJ 2020, 'Symbiodiniaceae-bacteria interactions: rethinking metabolite exchange in reef-building corals as multi-partner metabolic networks', ENVIRONMENTAL MICROBIOLOGY, vol. 22, no. 5, pp. 1675-1687.View/Download from: Publisher's site
Pernice, M, Raina, J-B, Rädecker, N, Cárdenas, A, Pogoreutz, C & Voolstra, CR 2020, 'Down to the bone: the role of overlooked endolithic microbiomes in reef coral health.', The ISME Journal: multidisciplinary journal of microbial ecology, vol. 14, no. 2, pp. 325-334.View/Download from: Publisher's site
Reef-building corals harbour an astonishing diversity of microorganisms, including endosymbiotic microalgae, bacteria, archaea, and fungi. The metabolic interactions within this symbiotic consortium are fundamental to the ecological success of corals and the unique productivity of coral reef ecosystems. Over the last two decades, scientific efforts have been primarily channelled into dissecting the symbioses occurring in coral tissues. Although easily accessible, this compartment is only 2-3 mm thick, whereas the underlying calcium carbonate skeleton occupies the vast internal volume of corals. Far from being devoid of life, the skeleton harbours a wide array of algae, endolithic fungi, heterotrophic bacteria, and other boring eukaryotes, often forming distinct bands visible to the bare eye. Some of the critical functions of these endolithic microorganisms in coral health, such as nutrient cycling and metabolite transfer, which could enable the survival of corals during thermal stress, have long been demonstrated. In addition, some of these microorganisms can dissolve calcium carbonate, weakening the coral skeleton and therefore may play a major role in reef erosion. Yet, experimental data are wanting due to methodological limitations. Recent technological and conceptual advances now allow us to tease apart the complex physical, ecological, and chemical interactions at the heart of coral endolithic microbial communities. These new capabilities have resulted in an excellent body of research and provide an exciting outlook to further address the functional microbial ecology of the "overlooked" coral skeleton.
Carney, RL, Brown, MV, Siboni, N, Raina, J-B, Kahlke, T, Mitrovic, SM & Seymour, JR 2020, 'Highly heterogeneous temporal dynamics in the abundance and diversity of the emerging pathogens Arcobacter at an urban beach', WATER RESEARCH, vol. 171.View/Download from: Publisher's site
Lawson, CA, Seymour, JR, Possell, M, Suggett, DJ & Raina, JB 2020, 'The Volatilomes of Symbiodiniaceae-Associated Bacteria Are Influenced by Chemicals Derived From Their Algal Partner', Frontiers in Marine Science, vol. 7.View/Download from: Publisher's site
© Copyright © 2020 Lawson, Seymour, Possell, Suggett and Raina. Biogenic volatile organic compounds (BVOCs) are a large group of molecules involved in trophic interactions, stress response and atmospheric chemistry. Although they have been extensively studied in terrestrial ecosystems, their identity and prevalence in the marine environment remains largely unexplored. Here we characterized the volatilome of two abundant marine bacteria that were previously identified as members of the core microbiome of Symbiodiniaceae (phylum: Dinoflagellata), the photosynthetic endosymbionts of reef building corals. To determine the influence of Symbiodiniaceae exudate on their associated bacteria, we incubated isolates of Marinobacter adhaerens HP15 and Labrenzia sp. 21p with Symbiodiniaceae culture filtrate or culture medium (control) and investigated their volatilomes using GC–MS. The volatilome of Labrenzia sp. incubated in Symbiodiniaceae filtrate was significantly different and more diverse relative to the control. In contrast, the overall composition of the M. adhaerens volatilomes were consistent between treatment and control. Among the 35 compounds detected in both bacterial species, the dominant chemical functional groups were halogenated hydrocarbons, aromatic hydrocarbons and organosulfurs, some of which are known to play roles in inter-organism signaling, to act as antioxidants and as antimicrobials. This study provides new insights into the potential sources and diversity of marine BVOCs, uncovering a wide range of molecules that may play important physiological and ecological roles for these organisms, while also revealing the role of Symbiodiniaceae-associated bacteria in the emission of important atmospheric gases.
Aguilar, C, Raina, J-B, Foret, S, Hayward, DC, Lapeyre, B, Bourne, DG & Miller, DJ 2019, 'Transcriptomic analysis reveals protein homeostasis breakdown in the coral Acropora millepora during hypo-saline stress', BMC GENOMICS, vol. 20.View/Download from: Publisher's site
Curson, ARJ, Williams, BT, Pinchbeck, BJ, Sims, LP, Martínez, AB, Rivera, PPL, Kumaresan, D, Mercadé, E, Spurgin, LG, Carrión, O, Moxon, S, Cattolico, RA, Kuzhiumparambil, U, Guagliardo, P, Clode, PL, Raina, J-B & Todd, JD 2019, 'Author Correction: DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton.', Nature microbiology, vol. 4, no. 3, pp. 540-542.View/Download from: Publisher's site
In the version of this Letter originally published, the Methods incorrectly stated that all phytoplankton cultures were sampled in mid-exponential phase. The low-nitrogen cultures were sampled in early stationary phase and at the point at which Fv/Fm values decreased, to indicate that cultures were experiencing low-nitrogen conditions. All other phytoplankton cultures were sampled in exponential phase. Growth and Fv/Fm data are provided here on high- and low-nitrogen cultures (Figs 1, 2 and 3) to clarify and support this correction. The Methods also stated that cell counting was done using a Beckman Multisizer 3 Coulter Counter, but a CASY Model TT Cell Counter was used.
Raina, J-B, Fernandez, V, Lambert, B, Stocker, R & Seymour, JR 2019, 'The role of microbial motility and chemotaxis in symbiosis.', Nature reviews. Microbiology, vol. 17, no. 5, pp. 284-294.View/Download from: Publisher's site
Many symbiotic relationships rely on the acquisition of microbial partners from the environment. However, the mechanisms by which microbial symbionts find and colonize their hosts are often unknown. We propose that the acquisition of environmental symbionts often necessitates active migration and colonization by the symbionts through motility and chemotaxis. The pivotal role of these behaviours in the onset and maintenance of symbiotic interactions is well established in a small number of model systems but remains largely overlooked for the many symbioses that involve the recruitment of microbial partners from the environment. In this Review, we highlight when, where and how chemotaxis and motility can enable symbiont recruitment and propose that these symbiont behaviours are important across a wide range of hosts and environments.
Lawson, CA, Possell, M, Seymour, JR, Raina, J-B & Suggett, DJ 2019, 'Coral endosymbionts (Symbiodiniaceae) emit species-specific volatilomes that shift when exposed to thermal stress.', Scientific reports, vol. 9, no. 1.View/Download from: Publisher's site
Biogenic volatile organic compounds (BVOCs) influence organism fitness by promoting stress resistance and regulating trophic interactions. Studies examining BVOC emissions have predominantly focussed on terrestrial ecosystems and atmospheric chemistry - surprisingly, highly productive marine ecosystems remain largely overlooked. Here we examined the volatilome (total BVOCs) of the microalgal endosymbionts of reef invertebrates, Symbiodiniaceae. We used GC-MS to characterise five species (Symbiodinium linucheae, Breviolum psygmophilum, Durusdinium trenchii, Effrenium voratum, Fugacium kawagutii) under steady-state growth. A diverse range of 32 BVOCs were detected (from 12 in D. trenchii to 27 in S. linucheae) with halogenated hydrocarbons, alkanes and esters the most common chemical functional groups. A thermal stress experiment on thermally-sensitive Cladocopium goreaui and thermally-tolerant D. trenchii significantly affected the volatilomes of both species. More BVOCs were detected in D. trenchii following thermal stress (32 °C), while fewer BVOCs were recorded in stressed C. goreaui. The onset of stress caused dramatic increases of dimethyl-disulfide (98.52%) in C. goreaui and nonanoic acid (99.85%) in D. trenchii. This first volatilome analysis of Symbiodiniaceae reveals that both species-specificity and environmental factors govern the composition of BVOC emissions among the Symbiodiniaceae, which potentially have, as yet unexplored, physiological and ecological importance in shaping coral reef community functioning.
Curson, ARJ, Williams, BT, Pinchbeck, BJ, Sims, LP, Martínez, AB, Rivera, PPL, Kumaresan, D, Mercadé, E, Spurgin, LG, Carrión, O, Moxon, S, Cattolico, RA, Kuzhiumparambil, U, Guagliardo, P, Clode, PL, Raina, J-B & Todd, JD 2018, 'DSYB catalyses the key step of dimethylsulfoniopropionate biosynthesis in many phytoplankton.', Nature microbiology, vol. 3, no. 4, pp. 430-439.View/Download from: Publisher's site
Dimethylsulfoniopropionate (DMSP) is a globally important organosulfur molecule and the major precursor for dimethyl sulfide. These compounds are important info-chemicals, key nutrients for marine microorganisms, and are involved in global sulfur cycling, atmospheric chemistry and cloud formation1-3. DMSP production was thought to be confined to eukaryotes, but heterotrophic bacteria can also produce DMSP through the pathway used by most phytoplankton 4 , and the DsyB enzyme catalysing the key step of this pathway in bacteria was recently identified 5 . However, eukaryotic phytoplankton probably produce most of Earth's DMSP, yet no DMSP biosynthesis genes have been identified in any such organisms. Here we identify functional dsyB homologues, termed DSYB, in many phytoplankton and corals. DSYB is a methylthiohydroxybutryate methyltransferase enzyme localized in the chloroplasts and mitochondria of the haptophyte Prymnesium parvum, and stable isotope tracking experiments support these organelles as sites of DMSP synthesis. DSYB transcription levels increased with DMSP concentrations in different phytoplankton and were indicative of intracellular DMSP. Identification of the eukaryotic DSYB sequences, along with bacterial dsyB, provides the first molecular tools to predict the relative contributions of eukaryotes and prokaryotes to global DMSP production. Furthermore, evolutionary analysis suggests that eukaryotic DSYB originated in bacteria and was passed to eukaryotes early in their evolution.
There are more than one million microbial cells in every drop of seawater, and their collective metabolisms not only recycle nutrients that can then be used by larger organisms but also catalyze key chemical transformations that maintain Earth's habitability. Understanding how these microbes interact with each other and with multicellular hosts is critical to reliably quantify any functional aspect of their metabolisms and to predict their outcomes on larger scales. Following a large body of literature pioneered by Farooq Azam and colleagues more than 30 years ago, I emphasize the importance of studying microbial interactions at the appropriate scale if we want to fully decipher the roles that they play in oceanic ecosystems.
Raina, J-B, Eme, L, Pollock, FJ, Spang, A, Archibald, JM & Williams, TA 2018, 'Symbiosis in the microbial world: from ecology to genome evolution.', Biology open, vol. 7, no. 2.View/Download from: Publisher's site
The concept of symbiosis - defined in 1879 by de Bary as 'the living together of unlike organisms' - has a rich and convoluted history in biology. In part, because it questioned the concept of the individual, symbiosis fell largely outside mainstream science and has traditionally received less attention than other research disciplines. This is gradually changing. In nature organisms do not live in isolation but rather interact with, and are impacted by, diverse beings throughout their life histories. Symbiosis is now recognized as a central driver of evolution across the entire tree of life, including, for example, bacterial endosymbionts that provide insects with vital nutrients and the mitochondria that power our own cells. Symbioses between microbes and their multicellular hosts also underpin the ecological success of some of the most productive ecosystems on the planet, including hydrothermal vents and coral reefs. In November 2017, scientists working in fields spanning the life sciences came together at a Company of Biologists' workshop to discuss the origin, maintenance, and long-term implications of symbiosis from the complementary perspectives of cell biology, ecology, evolution and genomics, taking into account both model and non-model organisms. Here, we provide a brief synthesis of the fruitful discussions that transpired.
van de Water, JAJM, Chaib De Mares, M, Dixon, GB, Raina, J-B, Willis, BL, Bourne, DG & van Oppen, MJH 2018, 'Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef-building coral.', Molecular ecology, vol. 27, no. 4, pp. 1065-1080.View/Download from: Publisher's site
Global increases in coral disease prevalence have been linked to ocean warming through changes in coral-associated bacterial communities, pathogen virulence and immune system function. However, the interactive effects of temperature and pathogens on the coral holobiont are poorly understood. Here, we assessed three compartments of the holobiont (host, Symbiodinium and bacterial community) of the coral Montipora aequituberculata challenged with the pathogen Vibrio coralliilyticus and the commensal bacterium Oceanospirillales sp. under ambient (27°C) and elevated (29.5 and 32°C) seawater temperatures. Few visual signs of bleaching and disease development were apparent in any of the treatments, but responses were detected in the holobiont compartments. V. coralliilyticus acted synergistically and negatively impacted the photochemical efficiency of Symbiodinium at 32°C, while Oceanospirillales had no significant effect on photosynthetic efficiency. The coral, however, exhibited a minor response to the bacterial challenges, with the response towards V. coralliilyticus being significantly more pronounced, and involving the prophenoloxidase-activating system and multiple immune system-related genes. Elevated seawater temperatures did not induce shifts in the coral-associated bacterial community, but caused significant gene expression modulation in both Symbiodinium and the coral host. While Symbiodinium exhibited an antiviral response and upregulated stress response genes, M. aequituberculata showed regulation of genes involved in stress and innate immune response processes, including immune and cytokine receptor signalling, the complement system, immune cell activation and phagocytosis, as well as molecular chaperones. These observations show that M. aequituberculata is capable of maintaining a stable bacterial community under elevated seawater temperatures and thereby contributes to preventing disease development.
Behrendt, L, Raina, J-B, Lutz, A, Kot, W, Albertsen, M, Halkjær-Nielsen, P, Sørensen, SJ, Larkum, AW & Kühl, M 2018, 'In situ metabolomic- and transcriptomic-profiling of the host-associated cyanobacteria Prochloron and Acaryochloris marina.', The ISME Journal, vol. 12, pp. 556-567.View/Download from: Publisher's site
The tropical ascidian Lissoclinum patella hosts two enigmatic cyanobacteria: (1) the photoendosymbiont Prochloron spp., a producer of valuable bioactive compounds and (2) the chlorophyll-d containing Acaryochloris spp., residing in the near-infrared enriched underside of the animal. Despite numerous efforts, Prochloron remains uncultivable, restricting the investigation of its biochemical potential to cultivation-independent techniques. Likewise, in both cyanobacteria, universally important parameters on light-niche adaptation and in situ photosynthetic regulation are unknown. Here we used genome sequencing, transcriptomics and metabolomics to investigate the symbiotic linkage between host and photoendosymbiont and simultaneously probed the transcriptional response of Acaryochloris in situ. During high light, both cyanobacteria downregulate CO2 fixing pathways, likely a result of O2 photorespiration on the functioning of RuBisCO, and employ a variety of stress-quenching mechanisms, even under less stressful far-red light (Acaryochloris). Metabolomics reveals a distinct biochemical modulation between Prochloron and L. patella, including noon/midnight-dependent signatures of amino acids, nitrogenous waste products and primary photosynthates. Surprisingly, Prochloron constitutively expressed genes coding for patellamides, that is, cyclic peptides of great pharmaceutical value, with yet unknown ecological significance. Together these findings shed further light on far-red-driven photosynthesis in natural consortia, the interplay of Prochloron and its ascidian partner in a model chordate photosymbiosis and the uncultivability of Prochloron.The ISME Journal advance online publication, 31 October 2017; doi:10.1038/ismej.2017.192.
Giardina, M, Cheong, S, Marjo, CE, Clode, PL, Guagliardo, P, Pickford, R, Pernice, M, Seymour, JR & Raina, J-B 2018, 'Quantifying Inorganic Nitrogen Assimilation by Synechococcus Using Bulk and Single-Cell Mass Spectrometry: A Comparative Study.', Frontiers in microbiology, vol. 9.View/Download from: Publisher's site
Microorganisms drive most of the major biogeochemical cycles in the ocean, but the rates at which individual species assimilate and transform key elements is generally poorly quantified. One of these important elements is nitrogen, with its availability limiting primary production across a large proportion of the ocean. Nitrogen uptake by marine microbes is typically quantified using bulk-scale approaches, such as Elemental Analyzer-Isotope Ratio Mass Spectrometry (EA-IRMS), which averages uptake over entire communities, masking microbial heterogeneity. However, more recent techniques, such as secondary ion mass spectrometry (SIMS), allow for elucidation of assimilation rates at the scale at which they occur: the single-cell level. Here, we combine and compare the application of bulk (EA-IRMS) and single-cell approaches (NanoSIMS and Time-of-Flight-SIMS) for quantifying the assimilation of inorganic nitrogen by the ubiquitous marine primary producer Synechococcus. We aimed to contrast the advantages and disadvantages of these techniques and showcase their complementarity. Our results show that the average assimilation of 15N by Synechococcus differed based on the technique used: values derived from EA-IRMS were consistently higher than those derived from SIMS, likely due to a combination of previously reported systematic depletion as well as differences in sample preparation. However, single-cell approaches offered additional layers of information, whereby NanoSIMS allowed for the quantification of the metabolic heterogeneity among individual cells and ToF-SIMS enabled identification of nitrogen assimilation into peptides. We suggest that this coupling of stable isotope-based approaches has great potential to elucidate the metabolic capacity and heterogeneity of microbial cells in natural environments.
Rädecker, N, Raina, J-B, Pernice, M, Perna, G, Guagliardo, P, Kilburn, MR, Aranda, M & Voolstra, CR 2018, 'Corrigendum: Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses.', Frontiers in physiology, vol. 9.View/Download from: Publisher's site
[This corrects the article on p. 214 in vol. 9, PMID: 29615919.].
Raedecker, N, Raina, J-B, Pernice, M, Perna, G, Guagliardo, P, Kilburn, MR, Aranda, M & Voolstra, CR 2018, 'Using Aiptasia as a Model to Study Metabolic Interactions in Cnidarian-Symbiodinium Symbioses', FRONTIERS IN PHYSIOLOGY, vol. 9.View/Download from: Publisher's site
Lawson, CA, Raina, J-B, Kahlke, T, Seymour, JR & Suggett, DJ 2018, 'Defining the core microbiome of the symbiotic dinoflagellate, Symbiodinium.', Environmental microbiology reports, vol. 10, no. 1, pp. 7-11.View/Download from: Publisher's site
Dinoflagellates of the genus Symbiodinium underpin the survival and ecological success of corals. The use of cultured strains has been particularly important to disentangle the complex life history of Symbiodinium and their contribution to coral host physiology. However, these cultures typically harbour abundant bacterial communities which likely play important, but currently unknown, roles in Symbiodinium biology. We characterized the bacterial communities living in association with a wide phylogenetic diversity of Symbiodinium cultures (18 types spanning 5 clades) to define the core Symbiodinium microbiome. Similar to other systems, bacteria were nearly two orders of magnitude more numerically abundant than Symbiodinium cells and we identified three operational taxonomic units (OTUs) which were present in all cultures. These represented the α-proteobacterium Labrenzia and the γ-proteobacteria Marinobacter and Chromatiaceae. Based on the abundance and functional potential of bacteria harboured in these cultures, their contribution to Symbiodinium physiology can no longer be ignored.
Aguilar, C, Raina, J-B, Motti, CA, Fôret, S, Hayward, DC, Lapeyre, B, Bourne, DG & Miller, DJ 2017, 'Transcriptomic analysis of the response of Acropora millepora to hypo-osmotic stress provides insights into DMSP biosynthesis by corals.', BMC Genomics, vol. 18, no. 1, pp. 1-14.View/Download from: Publisher's site
Dimethylsulfoniopropionate (DMSP) is a small sulphur compound which is produced in prodigious amounts in the oceans and plays a pivotal role in the marine sulfur cycle. Until recently, DMSP was believed to be synthesized exclusively by photosynthetic organisms; however we now know that corals and specific bacteria can also produce this compound. Corals are major sources of DMSP, but the molecular basis for its biosynthesis is unknown in these organisms.Here we used salinity stress, which is known to trigger DMSP production in other organisms, in conjunction with transcriptomics to identify coral genes likely to be involved in DMSP biosynthesis. We focused specifically on both adults and juveniles of the coral Acropora millepora: after 24 h of exposure to hyposaline conditions, DMSP concentrations increased significantly by 2.6 fold in adult corals and 1.2 fold in juveniles. Concomitantly, candidate genes enabling each of the necessary steps leading to DMSP production were up-regulated.The data presented strongly suggest that corals use an algal-like pathway to generate DMSP from methionine, and are able to rapidly change expression of the corresponding genes in response to environmental stress. However, our data also indicate that DMSP is unlikely to function primarily as an osmolyte in corals, instead potentially serving as a scavenger of ROS and as a molecular sink for excess methionine produced as a consequence of proteolysis and osmolyte catabolism in corals under hypo-osmotic conditions.
Seymour, JR, Amin, SA, Raina, J & Stocker, R 2017, 'Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships', Nature Microbiology, vol. 2, pp. 1-12.View/Download from: Publisher's site
By controlling nutrient cycling and biomass production at the base of the food web, interactions between phytoplankton and
bacteria represent a fundamental ecological relationship in aquatic environments. Although typically studied over large spatiotemporal
scales, emerging evidence indicates that this relationship is often governed by microscale interactions played out
within the region immediately surrounding individual phytoplankton cells. This microenvironment, known as the phycosphere,
is the planktonic analogue of the rhizosphere in plants. The exchange of metabolites and infochemicals at this interface governs
phytoplankton–bacteria relationships, which span mutualism, commensalism, antagonism, parasitism and competition. The
importance of the phycosphere has been postulated for four decades, yet only recently have new technological and conceptual
frameworks made it possible to start teasing apart the complex nature of this unique microbial habitat. It has subsequently
become apparent that the chemical exchanges and ecological interactions between phytoplankton and bacteria are far more
sophisticated than previously thought and often require close proximity of the two partners, which is facilitated by bacterial colonization
of the phycosphere. It is also becoming increasingly clear that while interactions taking place within the phycosphere
occur at the scale of individual microorganisms, they exert an ecosystem-scale influence on fundamental processes including
nutrient provision and regeneration, primary production, toxin biosynthesis and biogeochemical cycling. Here we review the
fundamental physical, chemical and ecological features of the phycosphere, with the goal of delivering a fresh perspective on
the nature and importance of phytoplankton–bacteria interactions in aquatic ecosystems.
Raina, J-B, Clode, PL, Cheong, S, Bougoure, J, Kilburn, MR, Reeder, A, Forêt, S, Stat, M, Beltran, V, Thomas-Hall, P, Tapiolas, D, Motti, CM, Gong, B, Pernice, M, Marjo, CE, Seymour, JR, Willis, BL & Bourne, DG 2017, 'Subcellular tracking reveals the location of dimethylsulfoniopropionate in microalgae and visualises its uptake by marine bacteria.', eLife, vol. 6, pp. 1-17.View/Download from: Publisher's site
Phytoplankton-bacteria interactions drive the surface ocean sulfur cycle and local climatic processes through the production and exchange of a key compound: dimethylsulfoniopropionate (DMSP). Despite their large-scale implications, these interactions remain unquantified at the cellular-scale. Here we use secondary-ion mass spectrometry to provide the first visualization of DMSP at sub-cellular levels, tracking the fate of a stable sulfur isotope ((34)S) from its incorporation by microalgae as inorganic sulfate to its biosynthesis and exudation as DMSP, and finally its uptake and degradation by bacteria. Our results identify for the first time the storage locations of DMSP in microalgae, with high enrichments present in vacuoles, cytoplasm and chloroplasts. In addition, we quantify DMSP incorporation at the single-cell level, with DMSP-degrading bacteria containing seven times more (34)S than the control strain. This study provides an unprecedented methodology to label, retain, and image small diffusible molecules, which can be transposable to other symbiotic systems.
Lambert, BS, Raina, J-B, Fernandez, VI, Rinke, C, Siboni, N, Rubino, F, Hugenholtz, P, Tyson, GW, Seymour, JR & Stocker, R 2017, 'A microfluidics-based in situ chemotaxis assay to study the behaviour of aquatic microbial communities.', Nature microbiology, vol. 2, pp. 1344-1349.View/Download from: Publisher's site
Microbial interactions influence the productivity and biogeochemistry of the ocean, yet they occur in miniscule volumes that cannot be sampled by traditional oceanographic techniques. To investigate the behaviours of marine microorganisms at spatially relevant scales, we engineered an in situ chemotaxis assay (ISCA) based on microfluidic technology. Here, we describe the fabrication, testing and first field results of the ISCA, demonstrating its value in accessing the microbial behaviours that shape marine ecosystems.A microfluidics-based assay for in situ chemotaxis experiments.
Gardner, SG, Raina, J-B, Nitschke, MR, Nielsen, DA, Stat, M, Motti, CA, Ralph, PJ & Petrou, K 2017, 'A multi-trait systems approach reveals a response cascade to bleaching in corals', BMC BIOLOGY, vol. 15.View/Download from: Publisher's site
Gardner, SG, Raina, J-B, Ralph, PJ & Petrou, K 2017, 'Reactive oxygen species (ROS) and dimethylated sulphur compounds in coral explants under acute thermal stress.', Journal of Experimental Biology, vol. 220, no. Pt 10, pp. 1787-1791.View/Download from: Publisher's site
Coral bleaching is intensifying with global climate change. Although the causes for these catastrophic events are well understood, the cellular mechanism that triggers bleaching is not well established. Our understanding of coral bleaching processes is hindered by the lack of robust methods for studying interactions between host and symbiont at the single-cell level. Here, we exposed coral explants to acute thermal stress and measured oxidative stress, more specifically, reactive oxygen species (ROS), in individual symbiont cells. Furthermore, we measured concentrations of dimethylsulphoniopropionate (DMSP) and dimethylsulphoxide (DMSO) to elucidate the role of these compounds in coral antioxidant function. This work demonstrates the application of coral explants for investigating coral physiology and biochemistry under thermal stress and delivers a new approach to study host-symbiont interactions at the microscale, allowing us to directly link intracellular ROS with DMSP and DMSO dynamics.
Jin, YK, Lundgren, P, Lutz, A, Raina, JB, Howell, EJ, Paley, AS, Willis, BL & van Oppen, MJH 2016, 'Genetic markers for antioxidant capacity in a reef-building coral', Science Advances, vol. 2, no. 5.View/Download from: Publisher's site
The current lack of understanding of the genetic basis underlying environmental stress tolerance in reef-building corals impairs the development of new management approaches to confronting the global demise of coral reefs. On the Great Barrier Reef (GBR), an approximately 51% decline in coral cover occurred over the period 1985–2012. We conducted a gene-by-environment association analysis across 12° latitude on the GBR, as well as both in situ and laboratory genotype-by-phenotype association analyses. These analyses allowed us to identify alleles at two genetic loci that account for differences in environmental stress tolerance and antioxidant capacity in the common coral Acropora millepora. The effect size for antioxidant capacity was considerable and biologically relevant (32.5 and 14.6% for the two loci). Antioxidant capacity is a critical component of stress tolerance because a multitude of environmental stressors cause increased cellular levels of reactive oxygen species. Our findings provide the first step toward the development of novel coral reef management approaches, such as spatial mapping of stress tolerance for use in marine protected area design, identification of stress-tolerant colonies for assisted migration, and marker-assisted selective breeding to create more tolerant genotypes for restoration of denuded reefs.
Raina, J, Tapiolas, D, Motti, CA, Foret, S, Seemann, T, Tebben, J, Willis, BL & Bourne, DG 2016, 'Isolation of an antimicrobial compoundproduced by bacteria associated withreef-building corals', PeerJ, vol. 4, pp. 1-20.View/Download from: Publisher's site
Bacterial communities associated with healthy corals produce antimicrobial
compounds that inhibit the colonization and growth of invasive microbes and
potential pathogens. To date, however, bacteria-derived antimicrobial molecules
have not been identified in reef-building corals. Here, we report the isolation of an
antimicrobial compound produced by Pseudovibrio sp. P12, a common and
abundant coral-associated bacterium. This strain was capable of metabolizing
dimethylsulfoniopropionate (DMSP), a sulfur molecule produced in high
concentrations by reef-building corals and playing a role in structuring their
bacterial communities. Bioassay-guided fractionation coupled with nuclear
magnetic resonance (NMR) and mass spectrometry (MS), identified the
antimicrobial as tropodithietic acid (TDA), a sulfur-containing compound likely
derived from DMSP catabolism. TDA was produced in large quantities by
Pseudovibrio sp., and prevented the growth of two previously identified coral
pathogens, Vibrio coralliilyticus and V. owensii, at very low concentrations
(0.5 mg/mL) in agar diffusion assays. Genome sequencing of Pseudovibrio sp. P12
identified gene homologs likely involved in the metabolism of DMSP and
production of TDA. These results provide additional evidence for the integral role of
DMSP in structuring coral-associated bacterial communities and underline the
potential of these DMSP-metabolizing microbes to contribute to coral disease
Rinke, C, Low, S, Woodcroft, BJ, Raina, J, Skarshewski, A, Le, XH, Butler, MK, Stocker, R, Seymour, JR, Tyson, GW & Hugenholtz, P 2016, 'Validation of picogram- and femtogram-input DNA libraries for microscale metagenomics', PeerJ, vol. 2016, no. 9.View/Download from: Publisher's site
High-throughput sequencing libraries are typically limited by the requirement for nanograms to micrograms of input DNA. This bottleneck impedes the microscale analysis of ecosystems and the exploration of low biomass samples. Current methods for amplifying environmental DNA to bypass this bottleneck introduce considerable bias into metagenomic profiles. Here we describe and validate a simple modification of the Illumina Nextera XT DNA library preparation kit which allows creation of shotgun libraries from sub-nanogram amounts of input DNA. Community composition was reproducible down to 100 fg of input DNA based on analysis of a mock community comprising 54 phylogenetically diverse Bacteria and Archaea. The main technical issues with the low input libraries were a greater potential for contamination, limited DNA complexity which has a direct effect on assembly and binning, and an associated higher percentage of read duplicates. We recommend a lower limit of 1 pg (∼100–1,000 microbial cells) to ensure community composition fidelity, and the inclusion of negative controls to identify reagent-specific contaminants. Applying the approach to marine surface water, pronounced differences were observed between bacterial community profiles of microliter volume samples, which we attribute to biological variation. This result is consistent with expected microscale patchiness in marine communities. We thus envision that our benchmarked, slightly modified low input DNA protocol will be beneficial for microscale and low biomass metagenomics.
D Ainsworth, T, Krause, L, Bridge, T, Torda, G, Raina, J-B, Zakrzewski, M, Gates, RD, Padilla-Gamiño, JL, Spalding, HL, Smith, C, Woolsey, ES, Bourne, DG, Bongaerts, P, Hoegh-Guldberg, O & Leggat, W 2015, 'The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts', ISME Journal, vol. 9, pp. 2261-2274.View/Download from: Publisher's site
Despite being one of the simplest metazoans, corals harbor some of the most highly diverse and abundant microbial communities. Differentiating core, symbiotic bacteria from this diverse host-associated consortium is essential for characterizing the functional contributions of bacteria but has not been possible yet. Here we characterize the coral core microbiome and demonstrate clear phylogenetic and functional divisions between the micro-scale, niche habitats within the coral host. In doing so, we discover seven distinct bacterial phylotypes that are universal to the core microbiome of coral species, separated by thousands of kilometres of oceans. The two most abundant phylotypes are co-localized specifically with the corals’ endosymbiotic algae and symbiont-containing host cells. These bacterial symbioses likely facilitate the success of the dinoflagellate endosymbiosis with corals in diverse environmental regimes.The ISME Journal advance online publication, 17 April 2015; doi:10.1038/ismej.2015.39.
Lutz, A, Raina, JB, Motti, CA, Miller, DJ & van Oppen, MJH 2015, 'Host Coenzyme Q Redox State Is an EarlyBiomarker of Thermal Stress in the CoralAcropora millepora', PLoS One, vol. 10, no. 10, pp. 1-18.View/Download from: Publisher's site
Bleaching episodes caused by increasing seawater temperatures may induce mass coral mortality and are regarded as one of the biggest threats to coral reef ecosystems worldwide. The current consensus is that this phenomenon results from enhanced production of harmful reactive oxygen species (ROS) that disrupt the symbiosis between corals and their endosymbiotic dinoflagellates, Symbiodinium. Here, the responses of two important antioxidant defence components, the host coenzyme Q (CoQ) and symbiont plastoquinone (PQ) pools, are investigated for the first time in colonies of the scleractinian coral, Acropora millepora, during experimentally-induced bleaching under ecologically relevant conditions. Liquid chromatography-mass spectrometry (LC-MS) was used to quantify the states of these two pools, together with physiological parameters assessing the general state of the symbiosis (including photosystem II photochemical efficiency, chlorophyll concentration and Symbiodinium cell densities). The results show that the responses of the two antioxidant systems occur on different timescales: (i) the redox state of the Symbiodinium PQ pool remained stable until twelve days into the experiment, after which there was an abrupt oxidative shift; (ii) by contrast, an oxidative shift of approximately 10% had occurred in the host CoQ pool after 6 days of thermal stress, prior to significant changes in any other physiological parameter measured. Host CoQ pool oxidation is thus an early biomarker of thermal stress in corals, and this antioxidant pool is likely to play a key role in quenching thermally-induced ROS in the coral-algal symbiosis. This study adds to a growing body of work that indicates host cellular responses may precede the bleaching process and symbiont dysfunction.
Garren, M, Son, K, Raina, J, Rusconi, R, Menolascina, F, Shapiro, H, Tout, JA, Bourne, DG, Seymour, JR & Stocker, R 2014, 'A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals', The ISME Journal, vol. 8, pp. 999-1007.View/Download from: Publisher's site
Diseases are an emerging threat to ocean ecosystems. Coral reefs, in particular, are experiencing a worldwide decline because of disease and bleaching, which have been exacerbated by rising seawater temperatures. Yet, the ecological mechanisms behind most coral diseases remain unidentified. Here, we demonstrate that a coral pathogen, Vibrio coralliilyticus, uses chemotaxis and chemokinesis to target the mucus of its coral host, Pocillopora damicornis. A primary driver of this response is the host metabolite dimethylsulfoniopropionate (DMSP), a key element in the global sulfur cycle and a potent foraging cue throughout the marine food web. Coral mucus is rich in DMSP, and we found that DMSP alone elicits chemotactic responses of comparable intensity to whole mucus. Furthermore, in heat-stressed coral fragments, DMSP concentrations increased fivefold and the pathogens chemotactic response was correspondingly enhanced. Intriguingly, despite being a rich source of carbon and sulfur, DMSP is not metabolized by the pathogen, suggesting that it is used purely as an infochemical for host location. These results reveal a new role for DMSP in coral disease, demonstrate the importance of chemical signaling and swimming behavior in the recruitment of pathogens to corals and highlight the impact of increased seawater temperatures on disease pathways.
Ceh, J, Kilburn, MR, Cliff, JB, Raina, J, van Keulen, M & Bourne, DG 2013, 'Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates', Ecology and Evolution, vol. 3, no. 8, pp. 2393-2400.View/Download from: Publisher's site
Raina, J, Tapiolas, DM, Foret, S, Lutz, A, Abrego, D, Ceh, J, Seneca, FO, Clode, PL, Bourne, DG, Willis, BL & Motti, CA 2013, 'DMSP biosynthesis by an animal and its role in coral thermal stress response', Nature, vol. 502, pp. 677-680.View/Download from: Publisher's site
Globally, reef-building corals are the most prolific producers of
dimethylsulphoniopropionate (DMSP)1,2, a central molecule in
the marine sulphur cycle and precursor of the climate-active gas
dimethylsulphide3,4. At present, DMSP production by corals is
attributed entirely to their algal endosymbiont, Symbiodinium2.
Combining chemical, genomic and molecular approaches, we show
that coral juveniles produce DMSP in the absence of algal symbionts.
DMSP levels increased up to 54% over time in newly settled
coral juveniles lacking algal endosymbionts, and further increases,
up to 76%, were recorded when juveniles were subjected to thermal
stress. We uncovered coral orthologues of two algal genes recently
identified in DMSP biosynthesis, strongly indicating that corals
possess the enzymatic machinery necessary for DMSP production.
Our results overturn the paradigm that photosynthetic organisms
are the sole biological source of DMSP, and highlight the double
jeopardy represented by worldwide declining coral cover, as the
potential to alleviate thermal stress through coral-produced DMSP
Tapiolas, DM, Raina, J, Lutz, A, Willis, BL & Motti, CA 2013, 'Direct measurement of dimethylsulfoniopropionate (DMSP) in reef-building corals using quantitative nuclear magnetic resonance (qNMR) spectroscopy', Journal of Experimental Marine Biology and Ecology, vol. 443, pp. 85-89.View/Download from: Publisher's site
Reef building corals are among the largest producers of dimethylsulfoniopropionate (DMSP), a sulfur molecule synthesized by their endosymbiotic dinoflagellates in the genus Symbiodinium. DMSP is potentially involved in important physiological and ecological processes in corals, but investigating the functional role of this molecule requires rapid and accurate quantification techniques. Here we introduce a simple method enabling direct quantification of DMSP and one of its breakdown products acrylate using quantitative nuclear magnetic resonance (qNMR) spectroscopy. The method was tested on a range of coral genera and presents a number of advantages over currently used quantification techniques, including simultaneous and direct quantification of multiple molecules from the same extract, and rapid processing with high reproducibility enabling analyses of large numbers of samples in short time periods. The method was successfully applied to environmental samples and provides the first baseline information on diel variation of DMSP and acrylate concentrations in the coral Acropora millepora.
Ceh, J, Raina, J, Soo, RM, van Keulen, M & Bourne, DG 2012, 'Coral-Bacterial Communities before and after a Coral Mass Spawning Event on Ningaloo Reef', PLoS One, vol. 7, no. 5.View/Download from: Publisher's site
Bacteria associated with three coral species, Acropora tenuis, Pocillopora damicornis and Tubastrea faulkneri, were assessed before and after coral mass spawning on Ningaloo Reef in Western Australia. Two colonies of each species were sampled before and after the mass spawning event and two additional samples were collected for P. damicornis after planulation. A variable 470 bp region of the 16 S rRNA gene was selected for pyrosequencing to provide an understanding of potential variations in coral-associated bacterial diversity and community structure. Bacterial diversity increased for all coral species after spawning as assessed by Chao1 diversity indicators. Minimal changes in community structure were observed at the class level and data at the taxonomical level of genus incorporated into a PCA analysis indicated that despite bacterial diversity increasing after spawning, coral-associated community structure did not shift greatly with samples grouped according to species. However, interesting changes could be detected from the dataset; for example, a-Proteobacteria increased in relative abundance after coral spawning and particularly the Roseobacter clade was found to be prominent in all coral species, indicating that this group may be important in coral reproduction.
Puill-Stephen, E, Willis, BL, Abrego, D, Raina, J & van Oppen, MJ 2012, 'Allorecognition maturation in the broadcast-spawning coral Acropora millepora', Coral Reefs, vol. 31, no. 4, pp. 1019-1028.View/Download from: Publisher's site
Many sessile marine invertebrates discriminate self from non-self with great precision, but maturation of allorecognition generally takes months to develop in juveniles. Here, we compare the development of allorecognition in full-sibling, half-sibling and non-sibling contact reactions between newly settled juveniles of the broadcast-spawning coral Acropora millepora on the Great Barrier Reef (Australia). Absence of a rejection response showed that A. millepora lacks a mature allorecognition system in the first 2 months post-settlement. From thereon, incompatibilities were observed between juveniles, their level of relatedness (i.e. full-, half- and non-sibling status) governing the rate of allorecognition maturation. All contact reactions between non-siblings resulted in rejections by 3 months post-settlement, whereas the expression of allorecognition took at least 5 months between half-siblings and longer than 13 months for some full-siblings. Approximately 74 % of fused full-siblings ( n = 19) persisted as chimeras at 11 months, thus maturation of allorecognition in this spawning coral appeared to be slower (>13 months) than in brooding corals (~4 months). We hypothesize that late maturation of allorecognition may contribute to flexibility in Symbiodinium uptake in corals with horizontal transmission, and could allow fusions and chimera formation in early ontogeny, which potentially enable rapid size increase through fusion
Raina, J, Dinsdale, EA, Willis, BL & Bourne, DG 2010, 'Do the organic sulfur compounds DMSP and DMS drive coral microbial associations?', Trends in Microbiology, vol. 18, no. 3, pp. 101-108.View/Download from: Publisher's site
Dimethylsulfoniopropionate (DMSP) and dimethylsulfide (DMS) are key compounds in the global sulfur cycle. Moreover, DMS is particularly important in climate regulation owing to its role in cloud formation. Reef building corals are major contributors to the production of these two compounds and also form diverse and complex associations with bacteria, which are known to play a crucial role in the degradation of DMSP and DMS. Here, we highlight an extensive overlap between bacterial species implicated in DMSP/DMS degradation and those associated with corals, leading to the hypothesis that these two compounds play a major role in structuring coral-associated bacterial communities, with important consequences for coral health and the resilience of coral reefs. We also explore the publically available metagenome databases and show that genes implicated in DMSP metabolism are abundant in the viral component of coral-reef-derived metagenomes, indicating that viruses can act as a reservoir for such genes.
Bartlett, CY, Manua, C, Cinner, J, Sutton, S, Jimmy, R, South, R, Nilson, J & Raina, J 2009, 'Comparison of Outcomes of Permanently Closed and Periodically Harvested Coral Reef Reserves', Conservation Biology, vol. 23, no. 6, pp. 1475-1484.View/Download from: Publisher's site
In many areas of the developing world, the establishment of permanent marine reserves is inhibited
by cultural norms or socioeconomic pressures. Community conserved areas that are periodically
harvested are increasingly being implemented as fisheries management tools, but few researchers have empirically
compared them with permanently closed reserves. We used a hierarchal control-impact experimental
design to compare the abundance and biomass of reef fishes, invertebrates, and substrate composition in
periodically harvested and permanent reserves and in openly fished (control sites) of the South Pacific island
country of Vanuatu. Fished species had significantly higher biomass in periodically harvested reserves than
in adjacent openly fished areas. We did not detect differences in substratum composition between permanent
reserves and openly fished areas or between permanent reserves and periodically harvested reserves. Giant
clams (tridacnids) and top shells (Trochus niloticus) were vulnerable to periodic harvest, and we suggest that
for adequate management of these species, periodically harvested community conservation areas be used in
conjunction with other management strategies. Periodic harvest within reserves is an example of adaptive
and flexible management that may meet conservation goals and that is suited to the social, economic, and
cultural contexts of many coastal communities in the developing world.
Cinner, JE, McClanahan, TR, Graham, NAJ, Pratchett, MS, Wilson, SK & Raina, J 2009, 'Gear-based fisheries management as a potential adaptive response to climate change and coral mortality', Journal of Applied Ecology, vol. 46, pp. 724-732.View/Download from: Publisher's site
Raina, J, Tapiolas, DM, Willis, BL & Bourne, DG 2009, 'Coral-associated bacteria and their role in the biogeochemical cycling of sulfur', Applied and Environmental Microbiology, vol. 75, no. 11, pp. 3492-3501.View/Download from: Publisher's site
Marine bacteria play a central role in the degradation of dimethylsulfoniopropionate (DMSP) to dimethyl
sulfide (DMS) and acrylic acid, DMS being critical to cloud formation and thereby cooling effects on the
climate. High concentrations of DMSP and DMS have been reported in scleractinian coral tissues although,
to date, there have been no investigations into the influence of these organic sulfur compounds on coralassociated
bacteria. Two coral species, Montipora aequituberculata and Acropora millepora, were sampled and
their bacterial communities were characterized by both culture-dependent and molecular techniques. Four
genera, Roseobacter, Spongiobacter, Vibrio, and Alteromonas, which were isolated on media with either DMSP or
DMS as the sole carbon source, comprised the majority of clones retrieved from coral mucus and tissue 16S
rRNA gene clone libraries. Clones affiliated with Roseobacter sp. constituted 28% of the M. aequituberculata
tissue libraries, while 59% of the clones from the A. millepora libraries were affiliated with sequences related
to the Spongiobacter genus. Vibrio spp. were commonly isolated from DMS and acrylic acid enrichments and
were also present in 16S rRNA gene libraries from coral mucus, suggesting that under ¿normal¿ environmental
conditions, they are a natural component of coral-associated communities. Genes homologous to dddD, and
dddL, previously implicated in DMSP degradation, were also characterized from isolated strains, confirming
that bacteria associated with corals have the potential to metabolize this sulfur compound when present in
coral tissues. Our results demonstrate that DMSP, DMS, and acrylic acid potentially act as nutrient sources
for coral-associated bacteria and that these sulfur compounds are likely to play a role in structuring bacterial
communities in corals, with important consequences for the health of both corals and coral reef ecosystems.