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Microbial interactions driven by organic and inorganic metabolic exchange and their role in present and future biogeochemical cycles

Periodic Reporting for period 1 - BioGeoMicrobes (Microbial interactions driven by organic and inorganic metabolic exchange and their role in present and future biogeochemical cycles)

Reporting period: 2022-12-01 to 2025-05-31

Marine micro-algae, particularly phytoplankton, play a crucial role in regulating the Earth's climate by acting as a significant sink for atmospheric carbon dioxide . Through photosynthesis, these organisms absorb CO2 and help mitigate its greenhouse effect, thus impacting global warming and climate change. This process is an essential part of the global carbon cycle. Micro-algae also interact with marine bacteria in complex chemical exchanges, which shape biogeochemical processes, including the carbon cycle and nutrient cycles, by influencing the movement and transformation of organic and inorganic compounds in marine environments.However despite recognition of the importance of algal-bacterial interactions in these processes, the molecular mechanisms underlying these exchanges remain poorly understood. As the ocean environment changes due to climate change—such as rising temperatures, acidification, and altered nutrient availability the dynamics of these interactions are also likely to change, potentially altering the functioning of biogeochemical cycles in ways that are not yet fully predictable.
This project seeks to comprehensively explore the interactions between marine micro-algae and bacteria, with a focus on understanding the organic and inorganic chemical exchanges that drive marine biogeochemical processes. The key objectives include:
1. Identification of Metabolites:which organic compounds, such as small molecules, metabolites, and signaling compounds, are exchanged between algae and bacteria in marine environments.
Investigating the exchange of inorganic molecules such as nitrogen species (e.g. nitrates, nitrites, ammonium), which are crucial for marine nutrient cycles and may be influenced by algal-bacterial interactions.
2. Investigating how both algae and bacteria respond physiologically to the metabolites exchanged between them. Including the impact on growth, metabolism, and survival.
3. Impact of Environmental Changes:Exploring how climate change-related alterations to ocean conditions—such as temperature increases, acidification, and nutrient imbalances might affect the nature and stability of algal-bacterial interactions. Will these critical processes persist under changing environmental conditions, or will new interactions emerge?The project aims to fill significant gaps in our understanding of the molecular and ecological mechanisms underlying algal-bacterial interactions.
The project will contribute to a more complete understanding of marine biogeochemical processes and a deeper understanding of how algal-bacterial interactions might change in the context of a warming and acidifying ocean.
The research conducted under the objectives of this funded project has been progressing successfully, yielding significant and publishable results in multiple areas.
We have identified various algal metabolites, including methylated compounds and vitamin D analogs, expanding our understanding of algal metabolism. These findings contributed to two major publications: Sperfeld et al. (2024) and Eliason et al. (2024). Additionally, we discovered that algae secrete inorganic nitrogen, a key process in nutrient dynamics and microbial interactions, which was published in Abada et al. (2023).
Our work also revealed bacterial nitric oxide secretion as a pathogenicity factor and characterized bacterial polysaccharides involved in biofilm formation, as detailed in Abada et al. (2023) and Lipsman et al. (2023), respectively. These findings highlight the role of microbial secretomes in modulating host-microbe interactions.
We demonstrated that bacterial communities exhibit altered pathogenic phenotypes when interacting with algae, as shown in Beiralas et al. (2023).
A major achievement is the creation of a novel dual RNA-Seq dataset, allowing for differential gene expression analysis in both algae and bacteria during co-cultivation. This dataset, alongside metabolomics analyses, provides insight into the molecular basis of algae-bacteria interactions, as detailed in Sperfeld et al. (2024).
We successfully introduced specific algal metabolites into bacterial cultures, leading to changes such as increased bacterial conjugation (Duchin Rapp et al., 2024), enhanced polysaccharide production (Lipsman et al., 2023), and accelerated bacterial growth during the lag phase (Sperfeld et al., 2024).
Our research uncovered a critical algal-bacterial-environmental circuit involving the methionine cycle, influencing both algal and bacterial metabolism (Sperfeld et al., 2024). Ongoing investigations focus on the role of inorganic hydrogen peroxide in these interactions.
We also demonstrated that increased UV exposure significantly affects the algal transcriptome and metabolome (Eliason et al., 2024), shedding light on algal stress responses and climate change adaptation. Elevated salinity was found to impact algal-bacterial interactions by increasing osmoprotectant production, as detailed in Sperfeld et al. (2024).
Additionally, we elucidated a previously unknown algal sterol biosynthesis pathway (Eliason et al., 2024), providing new insights into algal biochemistry and its ecological roles. Finally, we have made progress in collecting environmental samples, with the first batch retrieved for analysis of natural variability in algal-bacterial interactions.
Two of our publications stand out as particularly groundbreaking, with the potential to significantly impact both scientific understanding and practical applications. The first, Sperfeld et al., 2024, Nature Microbiology, uncovers a previously unknown aspect of bacterial physiology: the ability of bacteria to adjust the length of their lag phase in response to algal-derived metabolites. This discovery is important because the lag phase, which occurs when bacteria adapt to new environments before rapid growth, has been poorly understood. Our finding that algae can influence this phase through specific metabolites opens new avenues for studying bacterial adaptation, especially in nutrient-limited conditions. This insight could be pivotal in ecological research and offers exciting possibilities for enhancing microbial growth in agriculture and industrial applications. In fact, we recently secured an ERC Proof of Concept grant (101146837, FastMicrobes) to explore the practical uses of this discovery.

The second publication, Lipsman et al., 2023, npj Biofilms and Microbiomes, reveals a novel interaction between algae and bacteria: the formation of extracellular matrices that combine both algal and bacterial components. This microbial collaboration, previously unknown, has significant biotechnological potential. These mixed matrices could be utilized in biofilm-based bioremediation or the development of new bio-materials. Additionally, they offer new insights into environmental processes like marine snow and mucilage formation. Understanding the dynamics of these algal-bacterial matrices could have broad implications for both environmental microbiology and industrial biotechnology.

To ensure the full uptake and success of these findings, further research is needed to better understand the molecular mechanisms behind these interactions. Additionally, access to funding, commercialization support, and a clear regulatory framework will be crucial for translating these discoveries into practical applications, particularly in the fields of agriculture, biotechnology, and environmental management.
Fibers of bacterial matrix (green) in an aggregate of microalgae (magenta)
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