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Oceanic photosynthetic picoeukaryotes make a significant contribution to global oceanic meta-metabolism, indicating that cellular and genome streamlining confer ecological success

D. Derilus, C. E. Burdyshaw, F. Pinero, S. E. Massey*

*Corresponding author:

ABSTRACT: 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 here we utilize shotgun data from the Tara Oceans database to better understand both their ecological and genomic features. The clustering of meta-metabolic networks constructed from shotgun data from 10 different sampling sites is influenced by the proportion of PPEs in the datasets. 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 shows little variation, including those lineages with reduced genome sizes. This indicates genome and cellular streamlining is not an adaptation to environmental parameters, but may rather be a community-driven effect. Lastly, 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 contamination of the dataset 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-metabolic capacity, with implications for better understanding carbon fixation, biogeochemical cycling and planetary self-regulation.