Notable predominant morphology of the smallest most abundant protozoa of the open ocean revealed by electron microscopy

Abstract

Abstract In the microbe-driven ecosystems of the open ocean, the small heterotrophic flagellates (sHF) are the chief microbial predators and recyclers of essential nutrients to phototrophic microbes. Even with intensive molecular phylogenetic studies of the sHF, the origins of their feeding success remain obscure because of limited understanding of their morphological adaptations to feeding. Here, we examined the sHF morphologies in the largest, most oligotrophic South Pacific and Atlantic (sub)tropical gyres and adjacent mesotrophic waters. On four research cruises, the sHF cells were flow cytometrically sorted from bacterioplankton and phytoplankton for electron microscopy. The sorted sHF comprised chiefly heterokont (HK) biflagellates and unikont choanoflagellates numerically at around 10-to-1 ratio. Of the four differentiated morphological types of HK omnipresent in the open ocean, the short-tinsel heterokont (stHK), whose tinsel flagellum is too short to propagate a complete wave, is predominant and a likely candidate to be the most abundant predator on Earth. Modeling shows that the described stHK propulsion is effective in feeding on bacterioplankton cells at low concentrations; however, owing to general prey scarcity in the oligotrophic ocean, selective feeding is unsustainable and omnivory is equally obligatory for the seven examined sHF types irrespective of their mode of propulsion.