Periodic Reporting for period 1 - VIBES (The impact of the viral shunt and its metabolic landscape on microbial lifestyles and the flow of carbon during algal blooms)
Reporting period: 2022-10-01 to 2025-03-31
Phytoplankton blooms are responsible for ~50% of global photosynthesis, and strongly influence biogeochemical cycles. Viral infection is a prevalent cause of bloom demise, releasing up to 25% of algal biomass to the dissolved organic material (DOM) pool, a process termed the ‘viral shunt’. This ecosystem pathway fuels the oceanic microbiome that short-circuits carbon transfer to grazers by recycling DOM, thus reducing carbon export to the deep ocean. Estimated at 662 Gt, DOM is one of the largest global inventories of carbon. Despite its huge ecological significance, we lack tools to detect and quantify the viral shunt in the natural environment or assess the impact of marine viruses on oceanic microbiomes and, consequently, their effect on carbon sequestration. In the VIBES project we aim to assess the impact of the viral shunt and its metabolic landscape on microbial lifestyles and the flow of carbon during algal blooms. Using cutting edge tools, we disentangle the complexity of the viral shunt and elucidate its impact on microbial lifestyles (mutualism and pathogenicity) during algal bloom demise. We generate experimental approaches to study bacterial lifestyles and uncover the chemical language that mediates them. These approaches include the establishment of synthetic communities of microbial isolates from oceanic blooms, the use of single-cell RNAseq to quantify host-pathogen interactions, and metabolomics to identify the unique chemical signals that govern microbial interactions. We apply these methods both under controlled lab-based experiments and during complex interactions in the ocean. Ultimately, VIBES will enable us to evaluate the importance of microscale tripartite interactions of alga-virus-bacteria to the fate of carbon in the ocean.
Our first goal is to define the microbiome that is unique to the cosmopolitan alga E. huxleyi. This alga displays massive blooms in the ocean that stretch over thousands of kilometers and can be seen from space. We have now generated an unique microbiome archive of samples collected from five E. huxleyi blooms in different oceanic provinces of the Atlantic Ocean from Iceland to Patagonia. We analyzed bacterial growth and diversity during induced blooms in a mesocosm setup in the Fjords of Bergen, using 16S rDNA. This setup enabled high temporal sampling which provided initial insights into the microbial composition at different phases of the blooms. Furthermore, we provided results on the composition of the planktonic and of the particle-associated microbiome in the bloom. The latter can shed light on the specific microbial community that regulates carbon export to the seabed. Furthermore, we revealed new players in the recycling of algal biomass during viral infection. These were a group of eukaryotic heterotrophs, called Thraustochytrids, that can rival the free-living bacteria as potential recyclers of dissolved organic matter (Vincent et al. Nature Communications 2023). Our next goal is to further define the unique microbiome of virus-induced bloom demise from several locations in the Atlantic Ocean and to better predict bacterial functional phenotypes and key metabolic pathways using metagenomics and metatranscriptomics.
Next, we aimed to examine the unique microbial lifestyle in response to the viral shunt and its derived metabolites. For this aim, we developed an innovative approach to study the microbial lifestyles of the bacteria that thrived on viral-derived DOM (vDOM). We collected and preserved a large archive of Bloom-Associated Microbiomes (BAMs) from E. huxleyi blooms across the Atlantic Ocean. As a foundation for this goal, we successfully generated a synthetic community composed of alga, viruses and bacteria isolated from E. huxleyi bloom, that reproduced the dynamics observed in the ocean. Intriguingly, we revealed that adding BAMs to virus-infected E. huxleyi enhanced lysis of the algal culture as compared to virus infection alone. This important phenotype was termed ‘synergy’, a phenomenon known from the biomedical field but was never investigated in the marine environment. We are currently performing population genetic analysis in order to gain insight into the main bacteria taxa that drive this process and to identify the key metabolic pathways that are tuned towards virus-induced bloom demise in a specialized microbiome.
One of the main aims of our project is to map the unique metabolic landscape of viral infection in algal blooms in the ocean. In our new study, we mapped the viral shunt in large-scale blooms across the Atlantic Ocean, by applying metabolic biomarkers that are highly specific to viral infection of coccolithophore blooms. Using these specific metabolites that are generated during host-virus interactions, we developed specific organohalogens as a novel group of metabolic biomarkers to virus-induced demise of E. huxleyi blooms in the ocean. These specific metabolic footprints enabled sensitive detection of infections in the natural environment akin to their use as a diagnostic tool in the biomedical field. We found these metabolites to be highly stable in the extracellular milieu, thus providing a sensitive metabolic signature to track the impact of viral lysis in the ocean.
Next, we aimed to examine the unique microbial lifestyle in response to the viral shunt and its derived metabolites. For this aim, we developed an innovative approach to study the microbial lifestyles of the bacteria that thrived on viral-derived DOM (vDOM). We collected and preserved a large archive of Bloom-Associated Microbiomes (BAMs) from E. huxleyi blooms across the Atlantic Ocean. As a foundation for this goal, we successfully generated a synthetic community composed of alga, viruses and bacteria isolated from E. huxleyi bloom, that reproduced the dynamics observed in the ocean. Intriguingly, we revealed that adding BAMs to virus-infected E. huxleyi enhanced lysis of the algal culture as compared to virus infection alone. This important phenotype was termed ‘synergy’, a phenomenon known from the biomedical field but was never investigated in the marine environment. We are currently performing population genetic analysis in order to gain insight into the main bacteria taxa that drive this process and to identify the key metabolic pathways that are tuned towards virus-induced bloom demise in a specialized microbiome.
One of the main aims of our project is to map the unique metabolic landscape of viral infection in algal blooms in the ocean. In our new study, we mapped the viral shunt in large-scale blooms across the Atlantic Ocean, by applying metabolic biomarkers that are highly specific to viral infection of coccolithophore blooms. Using these specific metabolites that are generated during host-virus interactions, we developed specific organohalogens as a novel group of metabolic biomarkers to virus-induced demise of E. huxleyi blooms in the ocean. These specific metabolic footprints enabled sensitive detection of infections in the natural environment akin to their use as a diagnostic tool in the biomedical field. We found these metabolites to be highly stable in the extracellular milieu, thus providing a sensitive metabolic signature to track the impact of viral lysis in the ocean.
The metabolic exchange between algae and bacteria is one of the most important trophic interactions in the ocean, responsible for the largest flux of fixed carbon from photosynthetic biomass to the ocean microbiome. Phytoplankton-bacterial interactions can span the spectrum of mutualistic to pathogenic lifestyles and are important drivers of algal bloom development and demise. Major efforts have been focused on the characterization of the mutualistic phenotype; however, it has recently become clear that bacteria can kill algae and utilize their derived metabolic resources. Nevertheless, elucidating the molecular mechanisms that underscore bacterial pathogenicity is still its infancy. Furthermore, we know little about the role and function of pathogenic bacteria in regulating cell fate and flux of nutrients in algal blooms. In recent years we discovered that some Roseobacter sp. isolated from E. huxleyi blooms display a lifestyle switch from mutualism to pathogenicity when co-culture in the lab. We used the Roseobacter Sulfitobacter D7, which display this “Jekyll-and-Hyde” phenotype towards E. huxleyi, as a model system and discovered how the bacteria is tuned to the physiological state of its algal host, mediated by metabolic exchange. By profiling the bacterial transcriptomics in response to alga exudates, we revealed two key algal-derived metabolites, DMSP thar induces pathogenicity, and benzoate that can drive the mutualistic state (Barak-Gavish et al. eLIFE 2023).
Our next goal is to reveal mechanism of bacterial pathogenicity and the molecular regulation of the shift in lifestyles. We conducted a large scale dual RNAseq study during a detailed dynamics of Sulfitobacter D7 and E. huxleyi interactions in both mutualistic and pathogenic phases. We are now mining this dataset in search genes that regulate pathogenicity of marine bacteria. The candidate genes will be a great source for future genetic manipulation and phenotyping and will provide potential gene markers to detect bacterial pathogenic activity in algal blooms. This is especially important in the era of climate change and ocean warming that aggravates the occurrence of marine diseases and can expand their prevalence.
Our next goal is to reveal mechanism of bacterial pathogenicity and the molecular regulation of the shift in lifestyles. We conducted a large scale dual RNAseq study during a detailed dynamics of Sulfitobacter D7 and E. huxleyi interactions in both mutualistic and pathogenic phases. We are now mining this dataset in search genes that regulate pathogenicity of marine bacteria. The candidate genes will be a great source for future genetic manipulation and phenotyping and will provide potential gene markers to detect bacterial pathogenic activity in algal blooms. This is especially important in the era of climate change and ocean warming that aggravates the occurrence of marine diseases and can expand their prevalence.