Microbial and Viral Genome and Proteome Nitrogen Demand Varies Across Multiple Spatial Scales Within a Marine Oxygen Minimum Zone

Abstract

Nutrient availability can significantly influence microbial genomic and proteomic streamlining, for example by selecting for lower nitrogen to carbon ratios. Oligotrophic open ocean microbes have streamlined genomic nitrogen requirements relative to their counterparts in nutrient-rich coastal waters. However, steep gradients in nutrient availability occur at meter- and even micron-level spatial scales. It is unclear if such gradients also structure genomic and proteomic stoichiometry. Focusing on the eastern tropical North Pacific oxygen minimum zone (OMZ), we use comparative metagenomics to examine how nitrogen availability shapes microbial and viral genome properties along the vertical gradient across the OMZ and between two size fractions distinguishing free-living versus particle-associated microbes. We find a substantial increase in nitrogen content of encoded proteins in particle-associated over free-living bacteria and archaea across nitrogen availability regimes over depth. Within each size-fraction, we find that bacterial and viral genomic nitrogen tends to increase with increasing nitrate concentrations with depth. In contrast to cellular genes, the nitrogen content of virus proteins does not differ between size fractions. We identified arginine as a key amino acid in modulating the C:N ratio of core genes for bacteria, archaea, and viruses. Functional analysis reveals that particle-associated bacterial metagenomes are enriched for genes involved in arginine metabolism and organic nitrogen compound catabolism. Our results are consistent with nitrogen streamlining in both cellular and viral genomes on spatial scales of meters to microns. These effects are similar in magnitude to those previously reported across scales of thousands of kilometers. IMPORTANCEThe genomes of marine microbes can be shaped by nutrient cycles, with ocean-scale gradients in nitrogen availability known to influence microbial amino acid usage. It is unclear, however, how genomic properties are shaped by nutrient changes over much smaller spatial scales, for example along the vertical transition into oxygen minimum zones (OMZs) or from the exterior to interior of detrital particles. Here, we measure protein nitrogen usage by marine bacteria, archaea, and viruses using metagenomes from the nitracline of the eastern tropical North Pacific OMZ including both particle-associated and non-associated biomass. Our results show higher genomic and proteomic nitrogen content in particle-associated microbes and at depths with higher nitrogen availability for cellular and viral genomes. This discovery suggests that stoichiometry influences microbial and viral evolution across multiple scales, including the micro- to millimeter scale associated with particle-associated versus free-living lifestyles.