Photosynthetic picoeukaryotes significantly affect global oceanic meta-metabolism: cellular and genome streamlining confer ecological success

Photosynthetic picoeukaryotes (PPEs) are characterized by a reduction in cell and genome size but are free living, in contrast to many other organisms that have undergone such reductions. The relative abundance of PPEs in the oceans remains to be determined, as do the evolutionary imperatives behind their cell and genome reduction. Their enigmatic nature may be deciphered through metagenomics approaches; consequently, we utilized shotgun data from the Tara Oceans database to better understand both their ecological and genomic features. The clustering of meta-metabolomic networks constructed from shotgun data from 10 different sampling sites was influenced by the proportion of PPEs in the data sets. This, along with the relative abundance of RUBISCO sequences belonging to PPEs, indicates that they have a significant effect on oceanic meta-metabolism, emphasizing the evolutionary success of the streamlining strategy. Using rRNA sequences extracted from the shotgun data, a global oceanic distribution of PPEs showed little variation, including those lineages with reduced genome sizes. This indicates that genome and cellular streamlining is not an adaptation to environmental parameters but may rather be a community-driven effect. Lastly, and surprisingly given their role as primary producers, PPEs were found to comprise only 2 to 49% (17% on average) of all picoeukaryotes across 93 metagenomes. We show that contamination of the data set by eukaryotes with larger cell sizes is not responsible for the anomaly, and so the observation remains to be explained. The approaches described here allow us to draw a direct link between taxonomic composition and meta-metabolomic capacity, with implications for better understanding carbon fixation, biogeochemical cycling, and planetary self-regulation.