Ecological relevance of nucleotide salvage pathways in aquatic environments: significance in microbial bioenergetics and nutrient dynamics

• Applicant: Professor Dr. Michael Pester, since 1/2024
• Subject Area: Microbial Ecology and Applied Microbiology
• Term: since 2020
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 445123226

A prevailing view of modern oceanography is that nutrients limit the production of biomass in large areas of the pelagic ocean. Although most attention has focused on the importance of inorganic nutrients such as nitrate, phosphate, and iron in limiting phytoplankton growth and primary production, data also suggest that limitation of dissolved organic matter (DOM) also constrains cell growth. DOM encompasses a complex heterogeneous solution of diverse biomolecules mainly derived from cellular metabolic contents released after the disruption of planktonic cells, with viral-mediated cell lysis contributing up to one-quarter of the marine DOM pool. Therefore, biological mechanisms that affect DOM dynamics are of particular interest in understanding the role aquatic systems play in the global nutrient cycles. One acknowledged but poorly characterized constituent of DOM likely influencing structure and function of bacterioplankton communities, however, is freely dissolved nucleotides and their derivatives. Despite the significance of nucleotides to cell growth and viability, the production of these biomolecules is metabolically and energetically very costly, demanding a significant fraction of the production capacities of living cells. In turn, this implies that de novo synthesis is quite literally, the growth-limiting step in prokaryotes and eukaryotes alike. The motivation for this study, therefore, is to elucidate whether the recycling of exogenous nucleotides via salvage pathways represents an energetically efficient mechanism supporting DNA replication and cell growth in aquatic systems. Previous studies suggested that freely dissolved nucleotides are rapidly turned over in the ocean. However, the key microbial players remain unresolved, posing the question of whether ecologically relevant bacterioplankton abundant in the ocean such as SAR11, Prochlorococcus, Roseobacter, and Nitrosopumilus recycle exogenous nucleotides. Preliminary results based on genomic and metatranscriptomic data suggest that the recycling of exogenous nucleotides is a genetic determinant of microbial community assembly in aquatic systems and a potential driving force in the growth of streamlined pelagic bacterioplankton. These initial findings now allow designing targeted field and lab experiments to test the hypothesis that key bacterioplankton naturally metabolize dissolved nucleotides for growth, energy and nutrient conservation, or both. In this research, we propose two urgent studies to move this objective forward: (1) characterize the interplay between virioplankton community dynamics, dissolved nucleotide fluxes, and the transcriptional landscape of nucleotide salvage metabolism in the Red Sea and Lake Constance, and (2) elucidate the role salvaged nucleotides play in cell growth, energy metabolism, and response to nutrient limitation based on pure culture experiments with ecologically relevant bacterioplankton species.

• DFG Programme: Research Grants
• Ehemaliger Antragsteller: Dr. David Kamanda Ngugi, until 1/2024