Marine phototroph-heterotroph interactions

The productivity of marine systems relies on the growth of phytoplankton (phototrophs) which are mainly limited by nutrient availability. Bacteria benefit from the organic matter released by the phototrophs, re-mineralising the scarce nutrients within the system and making them available again to the phytoplankton (Christie-Oleza et al., 2017b). Nevertheless, other positive phototroph-heterotroph interactions have been described (i.e. the Black Queen Hypothesis) in Morris et al. (2012) based on vitamin exchange and alleviation of oxidative stress. Negative interactions such as competition for limited nutrients have also been reported (Thingstad et al., 1993) which is represented by the Red Queen Hypothesis as an evolutionary race. Here, nine phototrophs and 14 heterotrophs were co-cultivated in one-to-one species combinations with the aim of detecting a general behaviour of interactions between marine microbes. The interaction established in each co-culture was characterised based on population abundance and time of survival in both natural oligotrophic (SW) and nutrient-enriched seawater (ESW), compared to mono-culture conditions. Four different types of interactions (i.e. positive, semi-positive, neutral and negative) were detected in the 126 co-culture combinations. Many interactions varied between nutrient conditions highlighting nutrient availability as a key player in establishing interactions, as well as the need to test microorganisms in natural SW to reach reliable conclusions. In order to deepen our understanding of phototroph-heterotroph interactions, the proteomic profile of the co-cultures of the model heterotroph R. pomeroyi with each one of the nine phototrophs was performed in SW conditions. In the presence of the phototrophs, R. pomeroyi showed generic responses (e.g. in amino-acid uptake and N- metabolism, urea metabolism, vitamin biosynthesis and scavenging for aromatic compounds and CO metabolism as energy sources) but also species-specific responses (e.g. the relief of P stress, the reduction of specific S compounds and oxidative stress responses). In return, the nine phototrophs reacted differently to the presence of R. pomeroyi, with some phototrophs relying on R. pomeroyi for key metabolic processes and reaching some level of metabolic coupling with the heterotroph. The magnitude of species-specificity in the interactions between phototrophs and heterotrophs in natural seawater demonstrates the complexity of the system and the usefulness of this data for the interpretation of global biogeochemical cycles

Nutrient recycling facilitates long-term stability of marine microbial phototroph–heterotroph interactions

Biological interactions underpin the functioning of marine ecosystems, be it via competition, predation, mutualism or symbiosis processes. Microbial phototroph–heterotroph interactions propel the engine that results in the biogeochemical cycling of individual elements, and they are critical for understanding and modelling global ocean processes. Unfortunately, studies thus far have focused on exponentially growing cultures in nutrient-rich media, meaning knowledge of such interactions under in situ conditions is rudimentary at best. Here, we have performed long-term phototroph–heterotroph co-culture experiments under nutrient-amended and natural seawater conditions, and show 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 show that although Synechococcus is highly specialized for carrying out photosynthesis and carbon fixation, it relies on the heterotroph to remineralize the inevitably leaked organic matter, making nutrients circulate in a mutualistic system. In this sense we challenge the general belief that marine phototrophs and heterotrophs compete for the same scarce nutrients and niche space, and instead suggest that these organisms more probably benefit from each other because of their different levels of specialization and complementarity within long-term stable-state systems

Phytoplankton trigger the production of cryptic metabolites in the marine actinobacterium Salinispora tropica

Filamentous members of the phylum Actinobacteria are a remarkable source of natural products with pharmaceutical potential. The discovery of novel molecules from these organisms is, however, hindered because most of the biosynthetic gene clusters (BGCs) encoding these secondary metabolites are cryptic or silent and are referred to as orphan BGCs. While co‐culture has proven to be a promising approach to unlock the biosynthetic potential of many microorganisms by activating the expression of these orphan BGCs, it still remains an underexplored technique. The marine actinobacterium Salinispora tropica, for instance, produces valuable compounds such as the anti‐cancer molecule salinosporamide but half of its putative BGCs are still orphan. Although previous studies have used marine heterotrophs to induce orphan BGCs in Salinispora, its co‐culture with marine phototrophs has yet to be investigated. Following the observation of an antimicrobial activity against a range of phytoplankton by S. tropica, we here report that the photosynthate released by photosynthetic primary producers influences its biosynthetic capacities with production of cryptic molecules and the activation of orphan BGCs. Our work, using an approach combining metabolomics and proteomics, pioneers the use of phototrophs as a promising strategy to accelerate the discovery of novel natural products from marine actinobacteria

Pili allow dominant marine cyanobacteria to avoid sinking and evade predation

How oligotrophic marine cyanobacteria position themselves in the water column is currently unknown. The current paradigm is that these organisms avoid sinking due to their reduced size and passive drift within currents. Here, we show that one in four picocyanobacteria encode a type IV pilus which allows these organisms to increase drag and remain suspended at optimal positions in the water column, as well as evade predation by grazers. The evolution of this sophisticated floatation mechanism in these purely planktonic streamlined microorganisms has important implications for our current understanding of microbial distribution in the oceans and predator–prey interactions which ultimately will need incorporating into future models of marine carbon flux dynamics

Feeding response of the calanoid copepod Clausocalanus furcatus (Brady, 1883) under distinct light conditions

International Symposium Aquatic Mesocosm Research: Recent achievements and future directions in Aquatic Mesocosm Research, 16-19 October 2012, Heraklion, Crete, GreecePeer reviewe

Light-induced changes on the feeding behaviour of the calanoid copepod Clausocalanus furcatus (Brady, 1883): evidence from a mesocosm study

14 pages, 4 figures, 4 tablesLight and nutrient availability are assumed to largely control the dynamics and trophic efficiency of marine planktonic food webs, and are expected to be influenced by climate change (i.e. changes in stratification due to global warming). During an 8-day mesocosm experiment, we investigated the propagation of light energy up to the copepod trophic level in ultra-oligotrophic Eastern Mediterranean waters. Using mesocosms with light treatments corresponding to ca. 40% (L1) and 4.5% (L4) of the incident light intensity (simulating light conditions at 10 and 50–60 m depths, respectively), we assessed the feeding behaviour of the dominant copepod Clausocalanus furcatus every second day. We hypothesized that increased availability of copepod food at higher light levels would result in increased copepod ingestion rates and selectivity. Our results showed that copepod prey (microbial biomass.5 mm) had only a small increase in the L1 and daily rations (DRs) of C. furcatus were similar among treatments (usually ,15% of body carbon). Nevertheless, microplankton was clearly selected in L1, having double the contribution in the DR of C. furcatus compared with L4. A more balanced selective feeding pattern was observed in L4, with nanoplankton also being important in the diet. An increase in the copepod stock in the L1 compared with L4, observed at the end of the experiment, is likely associated with the light-mediated effects on C. furcatus feeding behaviour. We suggest that the importance of light availability on the efficiency of the marine planktonic food web should be further considered by climate change predictive modelsThis work was supported by the projects LightCopFed, LiMic, LightDynamix and from the European Union Seventh Framework Program (FP7/2007-2013) under grant agreement no. 228224, MESOAQUA, assigned to S.I. (LightCopFed), A.C. (LiMic), R.P., R.P (LightDynamix). R.P. acknowledges additional financial support by the German Research Council (DFG Pt 5/ 3-1)Peer reviewe

Effects of light availability on mixotrophy and microzooplankton grazing in an oligotrophic plankton food web: Evidences from a mesocosm study in Eastern Mediterranean waters

12 pages, 9 figures, 2 tablesPlankton biomass and composition in the pelagic zone of oceans is exposed to changes in availability of light and nutrients due to large-scale ocean circulation and water column stratification. We hypothesized that displacement of plankton from surface to deeper darker waters would not only favor heterotrophy over time, as previously suggested, but also first rapidly affect the level of mixotrophy and, consequently, overall microbial grazing in plankton food webs. To test this in an oligotrophic marine system we incubated Eastern Mediterranean water (from 10 m depth north of Crete in September 2010) in 2.8 m3 mesocosms simulating two different light intensities at the sampling station, surface waters (ca. 10 m; mesocosms L1) and deeper layers (ca. 50–60 m; mesocosms L4). The biomass and abundance of the main planktonic groups were monitored either daily or every second day, depending on the group. Microzooplankton grazing rates and the contribution of mixotrophic feeding were estimated by a combination of dilution experiments and incubations with live fluorescently labeled algae (LFLA). Although no nutrients were added to the mesocosms the chlorophyll a increased during the first 2 days of the experiment in both treatments. This increase resulted from phytoplankton growth in the light L1-mesocosm (autotrophic biomass was ca. doubled in L1 compared to L4), but was mostly due to photoadaptation of the algae in the L4-mesocosm, as indicated by lower carbon to chlorophyll a ratios. By the end of the experiment, the total biomass of protozoan and metazoan grazers in L1 was ca. twofold higher than in L4. The microzooplankton responded within the first 24 h, showing different grazing activity in L1 than in L4. Microzooplankton grazing rates on total Chl a were similar in both treatments; however, phytoplankton instantaneous growth rates were higher in the more illuminated mesocosm. This resulted in a closer coupling between both rates in L4, where all production was grazed daily, than in L1. Nevertheless, the overall flux of carbon through the microzooplankton was 33–60% higher in L1 compared to L4 throughout the experiment. The fraction of mixotrophy in the ciliate community varied in L1 (20–50%), but decreased over time in L4 from 50% to 30%. Our results do not support studies from freshwater, postulating that reduced light and nutrient limitation may increase herbivore production due to stoichiometric effects. Finally, we discuss how mixotrophy may bias rate estimates in dilution experimentsThis work was funded through projects CTM2009-08783 from the SpanishMinistry of Science and Innovation assigned to A.C. and projects LightDynamix, LiMic and LightCopFed from the European Union Seventh Framework Program (FP7/2007-2013) under grant agreement no. 228224, MESOAQUA, assigned to R.P. (LightDynamix), A.C., R.A.M., A.S., A.G. (LiMic) and S.I. (LightCopFed)Peer reviewe

From pico- to micro: variability of a spring bloom in an estuarine bay at a high temporal and spatial resolution

Aquatic Sciences Meeting, Aquatic Sciences: Global And Regional Perspectives - North Meets South, 22-27 February 2015, Granada, SpainPredicting the occurrence of Harmful Algal Blooms (HABs) in coastal ecosystems is crucial for their management. We followed up on the results of recent long-term data series and modelling studies of Alfacs Bay (Ebro Delta, Spain), an important aqua-/agricultural site and national park, recurrently threatened by HABs, to validate the previous results on a high spatio-temporal resolution, across a range of trophic levels. In 10 weekly cruises, we investigated the variability of the plankton community, including hetero- and autotrophic bacteria, nanoflagellates, and all sizes of phytoplankton as well as microzooplankton, sampling every meter of the shallow water column at a central station. Data on phytoplankton pigments and nutrients, as well as meteorological and hydrographic (using CTD and deployed sensors) parameters were recorded. Additionally, we conducted a 6-point-transect, taking CTD, nutrient and phytoplankton data. We discuss the high variability of the plankton community, the surprising importance of nanoflagellates, the influence of grazing and mixotrophy, the invasion of Mnemiopsis leydii and the culture of Mytilus edulis as possible factors for bloom development and evaluate how our data relate to the model-generated hypothesesPeer Reviewe

Effects of light availability on mixotrophy and microzooplankton grazing in an oligotrophic plankton food web: evidences from a mesocosm study in Eastern Mediterranean waters

International Symposium Aquatic Mesocosm Research: Recent achievements and future directions in Aquatic Mesocosm Research, 16-19 October 2012, Heraklion, Crete, GreecePeer Reviewe

Making in silico predictive models for toxicology FAIR

In silico predictive models for toxicology include quantitative structure-activity relationship (QSAR) and physiologically based kinetic (PBK) approaches to predict physico-chemical and ADME properties, toxicological effects and internal exposure. Such models are used to fill data gaps as part of chemical risk assessment. There is a growing need to ensure in silico predictive models for toxicology are available for use and that they are reproducible. This paper describes how the FAIR (Findable, Accessible, Interoperable, Reusable) principles, developed for data sharing, have been applied to in silico predictive models. In particular, this investigation has focussed on how the FAIR principles could be applied to improved regulatory acceptance of predictions from such models. Eighteen principles have been developed that cover all aspects of FAIR. It is intended that FAIRification of in silico predictive models for toxicology will increase their use and acceptance.This research received funding from the Innovative Medicines Initiative 2 Joint Undertaking (IMI2 JU) under grant agreement eTRANSAFE (777365), the European Union’s Horizon 2020 ELIXIR-CONVERGE Project (871075) and research and innovation programme under grant agreement No 964537 (RISK-HUNT3R)