Abstract
Many marine microbial eukaryotes combine photosynthetic with phagotrophic nutrition, but incomplete understanding of such mixotrophic protists, their functional diversity, and underlying physiological mechanisms limits the assessment and modeling of their roles in present and future ocean ecosystems. We developed an experimental system to study responses of mixotrophic protists to availability of living prey and light, and used it to characterize contrasting physiological strategies in two stramenopiles in the genus Ochromonas. We show that oceanic isolate CCMP1393 is an obligate mixotroph, requiring both light and prey as complementary resources. Interdependence of photosynthesis and heterotrophy in CCMP1393 comprises a significant role of mitochondrial respiration in photosynthetic electron transport. In contrast, coastal isolate CCMP2951 is a facultative mixotroph that can substitute photosynthesis by phagotrophy and hence grow purely heterotrophically in darkness. In contrast to CCMP1393, CCMP2951 also exhibits a marked photoprotection response that integrates non‐photochemical quenching and mitochondrial respiration as electron sink for photosynthetically produced reducing equivalents. Facultative mixotrophs similar to CCMP2951 might be well adapted to variable environments, while obligate mixotrophs similar to CCMP1393 appear capable of resource efficient growth in oligotrophic ocean environments. Thus, the responses of these phylogenetically close protists to the availability of different resources reveals niche differentiation that influences impacts in food webs and leads to opposing carbon cycle roles.
Highlights
Many marine microbial eukaryotes combine photosynthetic with phagotrophic nutrition, but incomplete understanding of such mixotrophic protists, their functional diversity, and underlying physiological mechanisms limits the assessment and modeling of their roles in present and future ocean ecosystems
Unicellular photosynthetic eukaryotes of diverse evolutionary origin have long been recognized as globally important primary producers in the ocean (Field et al 1998). These pigmented protists are clearly distinguished from purely heterotrophic protists, which are considered the major predators in marine microbial food webs, recycling nutrients, and linking bacterial production to higher trophic levels (Pomeroy 1974, Azam et al 1983)
Chrysophyte sequences retrieved from environmental assays are typically dominated by environmental clades (Lepere et al 2009, del Campo and Massana 2011), and the roles of individual clades in the marine microbial food web remain unknown
Summary
Many marine microbial eukaryotes combine photosynthetic with phagotrophic nutrition, but incomplete understanding of such mixotrophic protists, their functional diversity, and underlying physiological mechanisms limits the assessment and modeling of their roles in present and future ocean ecosystems. Mixotrophs can be important consumers of prokaryotic and eukaryotic microbes (Havskum and Hansen 1997, Sanders et al 2000, Unrein et al 2007, Hartmann et al 2012, Orsi et al 2018), but their concurrent contributions to carbon fixation via photosynthesis complicate integration of their ecosystem roles into biogeochemical models (Mitra et al 2014, Worden et al 2015) When both processes are integrated within the same cell, photosynthetic energy acquisition can compensate respirational losses of ingested carbon (Stoecker and Michaels 1991) leading to higher carbon transfer efficiencies from prey to predator, which is predicted to result in more productive food chains (Ward and Follows 2016). Ochromonas as defined today appears to be polyphyletic (Grossmann et al 2016) and the physiology of marine isolates has yet to be directly compared in feeding experiments
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