Evolutionary diversification of tiny ocean predators

Abstract

ABSTRACTUnicellular eukaryotic predators have a crucial role in the functioning of the ocean ecosystem by recycling nutrients and energy that are channeled to upper trophic levels. Traditionally, these evolutionary-diverse organisms have been combined into a single functional group (Heterotrophic flagellates), overlooking their organismal differences. Here we investigate four evolutionary related species belonging to one cosmopolitan family of uncultured marine picoeukaryotic predators: MAST-4 (species A, B, C, and E). Co-occurrence and distribution analyses in the global surface ocean indicated contrasting patterns in MAST-4A & C, suggesting adaptation to different temperatures. We then investigated whether these spatial distribution patterns were mirrored by MAST-4 genomic content using Single-Cell Genomics. Analyses of 69 single-cells recovered 66-83% of the MAST-4A/B/C/E genomes, which displayed substantial inter-species divergence. MAST-4 genomes were similar in terms of broad gene functional categories, but they differed in enzymes of ecological relevance, such as glycoside hydrolases (GHs), which are part of the food degradation machinery in MAST-4. Interestingly, MAST-4 species featuring a similar GH composition co-excluded each other (A & C) in the surface global ocean, while species with a different set of GHs appeared to be able to co-exist (species B & C) suggesting further niche diversification associated to prey digestion. We propose that differential niche adaptation to temperature and prey type has promoted adaptive evolutionary diversification in MAST-4. Altogether, we show that minute ocean predators from the same family may have different biogeography and genomic content, which need to be accounted to better comprehend marine food webs.