Strombidium rassoulzadegani: A Model Species for Chloroplast Retention in Oligotrich Ciliates

Abstract

Strombidium rassoulzadegani is a planktonic ciliate that retains chloroplasts from its food and uses them to obtain a nutritional supplement from photosynthesis. Unlike most members of the Oligotrichia, it is not difficult to grow in culture and thus it can serve as an experimental model for this kind of mixotrophy. We report here on its distribution, seasonal pattern of occurrence in the western North Atlantic, and on experiments to elucidate patterns of encystment and excystment, preferred food algae, and heterotrophic growth. Among ten different microalgae, including members of the Dinophyceae, Chlorophyceae, Haptophyceae, Cryptophyceae, and Bacillariophyceae, only four could support growth for more than 1 week, and only the chlorophyte Tetraselmis chui (PLY 429) could consistently support sustained growth in the dark. Of the four algae that supported growth, three also resulted in longer survival when the ciliate was subsequently starved in the light, compared to the dark, suggesting that all of them provided some photosynthetic benefit to the ciliate. The dinoflagellate Prorocentrum minimum (JA) supported similar survival in the light and dark and likely does not undergo chloroplast retention in the ciliate.

Metabolic Reliance on Photosynthesis Depends on Both Irradiance and Prey Availability in the Mixotrophic Ciliate, Strombidium cf. basimorphum

“…Mortality rates > 90% were only reached after 11 and 13 days, respectively (Figure 2B). This is in accordance with observations made on other generalist nonconstitutive mixotrophs (GNCMs) (Schoener and Mcmanus, 2012;Mcmanus et al, 2018;Maselli et al, 2020). This prolonged survival without access to prey stands in contrast to purely heterotrophic oligotrichs, which have been shown to reach almost complete culture mortality within 1-4 days (Montagnes, 1996).…”

“…Unlike the red Mesodinium spp., the mixotrophic oligotrichs have been shown to retain and utilize chloroplasts from many different species of algal prey (Johnson and Beaudoin, 2019;Maselli et al, 2020), and thus, are generally considered GNCMs. Mixotrophic oligotrichs are believed to depend on frequent reacquisition of prey plastids, as they do not appear to express genes related to plastid maintenance and replication (Santoferrara et al, 2014;Mcmanus et al, 2018). These plastidic oligotrichs make up, on average, 30% of ciliate biomass (Dolan and Pérez, 2000;Stoecker et al, 2009), and during spring-and summer-time peaks, they can even comprise >90% of ciliate biomass (Bernard and Rassoulzadegan, 1994;Haraguchi et al, 2018).…”

Annual Protist Community Dynamics in a Freshwater Ecosystem Undergoing Contrasted Climatic Conditions: The Saint-Charles River (Canada)

“…From autotrophy (photosynthesizers) to heterotrophy (predators feeding on other eukaryotic or prokaryotic organisms, decomposers, saprophytes, and parasites of other organisms), through mixotrophy, protists cover multiple ecological roles in ecosystems (Arndt et al, 2000; Zubkov and Tarran, 2008). While it was commonly accepted that some eukaryotic phyla were strictly photosynthetic or phagotrophic, numerous studies have demonstrated that many groups are actually more flexible in their nutritional capabilities than initially thought (Laval-Peuto and Febvre, 1986; McManus and Fuhrman, 1986; Stoecker and Silver, 1987; McManus et al, 2018). For example, photosynthetic capability via endosymbiotic associations or chloroplast retention (uptake of chloroplast from their prey, or kleptoplasty) has been observed in a broad range of eukaryotic lineages, such as ciliates, that were previously associated with a phagotrophic non-photosynthetic lifestyle (Stoecker and Silver, 1987; Dolan, 1992; Johnson, 2011; McManus et al, 2018) or dinoflagellates (Minnhagen et al, 2008; Hansen et al, 2016).…”

“…While it was commonly accepted that some eukaryotic phyla were strictly photosynthetic or phagotrophic, numerous studies have demonstrated that many groups are actually more flexible in their nutritional capabilities than initially thought (Laval-Peuto and Febvre, 1986; McManus and Fuhrman, 1986; Stoecker and Silver, 1987; McManus et al, 2018). For example, photosynthetic capability via endosymbiotic associations or chloroplast retention (uptake of chloroplast from their prey, or kleptoplasty) has been observed in a broad range of eukaryotic lineages, such as ciliates, that were previously associated with a phagotrophic non-photosynthetic lifestyle (Stoecker and Silver, 1987; Dolan, 1992; Johnson, 2011; McManus et al, 2018) or dinoflagellates (Minnhagen et al, 2008; Hansen et al, 2016). Likewise, the loss of chloroplasts by lineages within commonly accepted photosynthetic groups has also been detected, such as the Paraphysomonas -clade within Chrysophyceae (Stramenopiles) (Caron et al, 1999; Boenigk et al, 2005; Scoble and Cavalier-Smith, 2014; Grossmann et al, 2016).…”

“…Likewise, the loss of chloroplasts by lineages within commonly accepted photosynthetic groups has also been detected, such as the Paraphysomonas -clade within Chrysophyceae (Stramenopiles) (Caron et al, 1999; Boenigk et al, 2005; Scoble and Cavalier-Smith, 2014; Grossmann et al, 2016). Mixotrophy, defined as the combination of phagotrophy and photosynthesis in an individual cell, is increasingly recognized as an important trophic mode among aquatic eukaryotes and is likely the rule rather than the exception in microbial food webs (Caron et al, 1999; Stoecker et al, 2017; McManus et al, 2018; Stoecker and Lavrentyev, 2018). In addition, bacterivorous eukaryotes do not feed equally on all microorganisms.…”