Abstract

Large swaths of the nutrient-poor surface ocean are dominated numerically by cyanobacteria (Prochlorococcus), cyanobacterial viruses (cyanophage), and alphaproteobacteria (SAR11). How these groups thrive in the diverse physicochemical environments of different oceanic regions remains poorly understood. Comparative metagenomics can reveal adaptive responses linked to ecosystem-specific selective pressures. The Red Sea is well-suited for studying adaptation of pelagic-microbes, with salinities, temperatures, and light levels at the extreme end for the surface ocean, and low nutrient concentrations, yet no metagenomic studies have been done there. The Red Sea (high salinity, high light, low N and P) compares favorably with the Mediterranean Sea (high salinity, low P), Sargasso Sea (low P), and North Pacific Subtropical Gyre (high light, low N). We quantified the relative abundance of genetic functions among Prochlorococcus, cyanophage, and SAR11 from these four regions. Gene frequencies indicate selection for phosphorus acquisition (Mediterranean/Sargasso), DNA repair and high-light responses (Red Sea/Pacific Prochlorococcus), and osmolyte C1 oxidation (Red Sea/Mediterranean SAR11). The unexpected connection between salinity-dependent osmolyte production and SAR11 C1 metabolism represents a potentially major coevolutionary adaptation and biogeochemical flux. Among Prochlorococcus and cyanophage, genes enriched in specific environments had ecotype distributions similar to nonenriched genes, suggesting that inter-ecotype gene transfer is not a major source of environment-specific adaptation. Clustering of metagenomes using gene frequencies shows similarities in populations (Red Sea with Pacific, Mediterranean with Sargasso) that belie their geographic distances. Taken together, the genetic functions enriched in specific environments indicate competitive strategies for maintaining carrying capacity in the face of physical stressors and low nutrient availability.

Highlights

  • A handful of dominant microbial groups are found consistently in the tropical and subtropical surface ocean

  • The Prochlorococcus populations are dominated by the high-light II (HLII) clade, ~80–95% in each sea except MED, where the high-light I (HLI) clade dominates

  • We expected to find direct adaptations for coping with high salinity, but what we found instead was a secondary effect: SAR11 consumes the osmolytes produced by Prochlorococcus and other phytoplankton to cope with high salinity

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Summary

Introduction

A handful of dominant microbial groups are found consistently in the tropical and subtropical surface ocean. Cyanobacteria of the genus Prochlorococcus, viruses (cyanophage) infecting Prochlorococcus, and proteobacteria of the SAR11 clade, together fill critical biogeochemical roles in primary production and cycling of carbon and nutrients. While these groups are ubiquitous, they are not homogenous. Populations in different seas and oceans exhibit phenotypes that reflect local environmental conditions, such as low nutrients, high salinity, or high irradiance. Community genomics (metagenomics) has become an important tool in marine microbial ecology, in the comparison of multiple environments (comparative metagenomics) to reveal adaptive genotypes.

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