Figure 1. Schematic representation of the nutrient circulation process taking place in marine phototroph (Synechococcus sp. WH7803)-heterotroph (R. pomeroyi DSS-3) co-cultures. Adapted from Christie-Oleza et al. 2017 Nature Microbiology, 2: 17100
Figure 3. Type IV pili in marine picocyanobacteria allow these planktonic marine microbes to avoid sinking and evade predation.
Publications issued from this work:
Christie-Oleza, J.A.; Armengaud, J.; Scanlan, D.J. 2015 Functional distinctness in the exoproteomes of marine Synechococcus. Environmental Microbiology, 17 (10): 3781-3794
Kaur, A., Hernandez-Fernaud, J.R., Aguilo-Ferretjans, M.M., Wellington, E.M., Christie-Oleza, J.A. 2017 100 days of marine Synechococcus - Ruegeria pomeroyi interaction, a detailed analysis of the exoproteome. Environmental Microbiology, doi: 10.1111/1462-2920.14012.
Aguilo-Ferretjans, M.M.; Bosch, R.; Puxty, R.J.; Latva, M.; Zadjelovic, V.; Chhun, A.; Sousoni, D.; Polin, M.; Scanlan, D.J.; Christie-Oleza, J.A.* 2021 Pili allow dominant marine cyanobacteria to avoid sinking and evade predation. Nature Communications, 12: 1857.
Publications issued from this work:
Chhun, A.; Sousoni, D.; Aguilo‐Ferretjans, M.M.; Song, L.; Corre, C.; Christie‐Oleza, J.A.* 2021 Phytoplankton trigger the production of cryptic metabolites in the marine actinobacterium Salinispora tropica. Microbial Biotechnology, 14: 291-306.
The secretion of metabolites is another way bacteria have to exert an influence on their surrounding microbes. The data generated by our group in collaboration with Dr Corre from the Department of Chemistry (University of Warwick) allowed the identification of, first, a novel polyketide produced by Synechococcus and, second, two metabolites secreted by the marine heterotroph Salinispora to kill cyanobacteria (Fig 4). But our interest is not limited to bacterial secondary metabolites as recent findings from our research have highlighted that metabolites from the central metabolism are leaked by phototrophic primary producers enhancing the cross-feeding with the heterotrophic community. Most interestingly, we have the hypothesis that some of these central metabolites have fascinating evolutionary implications that links the central metabolism to other key metabolic processes that were thought to be lacking in marine picocyanobacteria.
Figure 4. Interaction of Salinispora tropica with phytoplankton. Marine phototrophs release photosynthate that triggers the biosynthesis of novel cryptic metabolites in S. tropica. S. tropica produces an unknown antimicrobial molecule that kills phytoplankton.
Despite being some of the most nutrient-depleted environments, open oceans remain highly productive. It has now been well documented that unicellular photosynthetic microbes that populate these vast pelagic areas fuel the entire marine engine. These small primary producers have evolved fascinating mechanisms to adapt to these extreme oligotrophic conditions and, still, remain highly active. As part of these adaptations, stable marine environments have also allowed marine microbes to evolve towards cooperative behaviours through mutualistic interactions. The study of microbial interactions is still in its infancy and further research is required for the full understanding of these complex systems in order to predict how climate change (i.e. temperature, nutrient availability due to water stratification and other variables) will influence future microbial assemblages.
Guided by this rationale, our lab is working on three topics within this line of research: nutrient cycling, exoproteomics and metabolomics. To learn more about these, click on the corresponding box.
Marine microbial interactions
Pushing evolution towards extreme oligotrophy
Microbial phototroph-heterotroph interactions propel the engine that results in the biogeochemical cycling of individual elements and are critical for understanding and modelling global ocean processes. In order to understand phototroph-heterotroph interactions, our group performed long-term phototroph-heterotroph co-culture experiments under nutrient-amended and natural seawater conditions which showed that it is not the concentration of nutrients but rather their circulation that maintains a stable interaction and a dynamic system.
Using the Synechococcus-Roseobacter interaction as a model phototroph-heterotroph case study we showed that whilst Synechococcus is highly specialised for carrying out photosynthesis and carbon-fixation it relies on the heterotroph to re-mineralise the inevitably leaked organic matter making nutrients circulate in a mutualistic system (Figure 1).
In this sense our research has challenged the general belief that marine phototrophs and heterotrophs compete for the same scarce nutrients and niche space, but instead suggests these organisms more likely benefit from each other because of their different levels of specialization and complementarity within long-term stable-state systems.
Publication issued from this work:
Christie-Oleza, J.A.; Sousoni, D.; Lloyd, M.; Armengaud, J.; Scanlan, D.J. 2017 Nutrient recycling facilitates long-term stability of marine microbial phototroph-heterotroph interactions. Nature Microbiology, 2: 17100.
Helliwell, K.E.; Harrison, E.L.; Christie-Oleza, J.A.; Rees, A.P.; Kleiner, F.H.; Gaikwad, T.; Downe, J.; Aguilo-Ferretjans, M.M.; Al-Moosawi, L.; Brownlee, C.; Wheeler, G.L. 2021 A novel Ca2+ signaling pathway coordinates environmental phosphorus sensing and nitrogen metabolism in marine diatoms. Current Biology, 31: 978-989.
The exoproteome is the protein fraction found in the extracellular proximity of one or several organisms and is generally a good indicator of their microbial lifestyle strategies.
Joseph has pioneered some of the first exoproteomic analyses on environmental marine microbes during one of his postdoctoral work in France. The bioinformatic prediction of the exported pan-proteome of marine picocyanobacteria (i.e. the Prochlorococcus and Synechococcus lineages) he performed as demonstrated that i) this fraction of the encoded proteome has a much higher incidence of lineage-specific proteins than the cytosolic fraction (57% and 73% homologue incidence, respectively), and ii) exported proteins are largely uncharacterized to date (54%) compared to proteins from the cytosolic fraction (35%). This suggests that the genomic and functional diversity of these organisms lies largely in the diverse pool of novel functions these organisms export to/through their membranes playing a key role in community diversification, e.g. for niche partitioning or evading predation.
Figure 2. Schematic representation of basic functions observed by exoproteomic analyses of phototroph-heterotroph interactions.
The experimental exoproteome analysis of marine Synechococcus has shown transport systems for inorganic nutrients, an interesting array of strain-specific exoproteins involved in mutualistic or hostile interactions (i.e. hemolysins, pilins, adhesins), and exoenzymes with a potential mixotrophic goal (i.e. exoproteases and chitinases) which are currently being further characterised in our laboratory (Figure 2). We have also shown how these organisms can remodel their exoproteome, i.e. by increasing the repertoire of interaction proteins when grown in the presence of a heterotroph or decrease exposure to prey when grown in the dark. We went on to analyse the exoproteome of different heterotrophic bacteria (i.e. Roseobacter isolates) when grown in the presence of Synechococcus and feed on their photosynthate. The primary produced organic matter is mostly re-mineralised by heterotrophic microorganisms but, because most of the oceanic dissolved organic matter (DOM) is in the form of biopolymers, and microbial membrane transport systems operate with molecules <0.6 kDa, it must be hydrolysed outside the cell before a microorganism can acquire it. This approach has identified the repertoire of hydrolytic enzymes secreted by Roseobacter, opening up the black box of heterotrophic transformation/re-mineralisation of biopolymers generated by marine phytoplankton. As well as highlighting interesting exoenzymes this strategy also allowed us to infer clues on the molecular basis of niche partitioning.
Type IV pili have been studied for decades as these thin proteinaceous filamentous appendages decorate the cell surface of a wide range of bacteria. Traditionally, type IV pili have been associated with twitching motility, surface attachment, biofilm formation, pathogenicity, as well as conjugation, exogenous DNA acquisition, competence and secretion. In our recent study published in Nature Communications [Aguilo-Ferretjans et al 2021] we provide yet another biological function to these filamentous appendages and shed light on the ecological role of type IV pili in marine ecosystems (Fig 3).