Decoupling of respiration rates and abundance in marine prokaryoplankton

The ocean-atmosphere exchange of CO2 largely depends on the balance between marine microbial photosynthesis and respiration. Despite vast taxonomic and metabolic diversity among marine planktonic bacteria and archaea (prokaryoplankton)(1-3), their respiration usually is measured in bulk and treated as a 'black box' in global biogeochemical models(4); this limits the mechanistic understanding of the global carbon cycle. Here, using a technology for integrated phenotype analyses and genomic sequencing of individual microbial cells, we show that cell-specific respiration rates differ by more than 1,000x among prokaryoplankton genera. The majority of respiration was found to be performed by minority members of prokaryoplankton (including the Roseobacter cluster), whereas cells of the most prevalent lineages (including Pelagibacter and SAR86) had extremely low respiration rates. The decoupling of respiration rates from abundance among lineages, elevated counts of proteorhodopsin transcripts in Pelagibacter and SAR86 cells and elevated respiration of SAR86 at night indicate that proteorhodopsin-based phototrophy(3,5-7) probably constitutes an important source of energy to prokaryoplankton and may increase growth efficiency. These findings suggest that the dependence of prokaryoplankton on respiration and remineralization of phytoplankton-derived organic carbon into CO2 for its energy demands and growth may be lower than commonly assumed and variable among lineages.

Automated summary

The respiration rates of marine microbes vary significantly among different prokaryoplankton genera. Minority members of prokaryoplankton perform the majority of respiration, while the most prevalent lineages have extremely low respiration rates. Proteorhodopsin-based phototrophy is likely an important source of energy for prokaryoplankton, indicating a need to reevaluate the mechanistic understanding of the global carbon cycle.