The genetic diversity of plastids associated with mixotrophic oligotrich ciliates

Abstract

Mixotrophic oligotrich ciliates use plastids sequestered from algal prey to acquire energy and metabolic products from photosynthesis. We isolated mixotrophic oligotrichs from coastal waters off Massachusetts (MA) and California (CA), as well as from two freshwater ponds in MA, and identified associated plastid 23S rRNA genes. Ciliates were identified using a combination of microscopy and 18S rRNA phylogeny, and included Laboea strobila and various Pseudotontonia, Spirotontonia, and Strombidium species from marine waters, and Limnostrombidium viride from freshwater. Overall, nearly half of all plastid sequences recovered from ciliates were haptophytes, followed by 15–20% for stramenopiles and chlorophytes, and < 10% originating from cryptophyte algae. No plastid sequences were from dinoflagellates. Cells of Strombidium ‘biarmatum’ collected from coastal MA in spring and fall possessed mostly Micromonas plastids, but during spring also possessed cryptophyte sequences. During spring, L. strobila were found to have a mix of chlorophyte, cryptophyte, haptophyte, and stramenopile sequences, while a co‐occurring Strombidium sp. had mostly chlorophyte and haptophyte sequences. Mixotrophic Pseudotontonia and Spirotontonia spp. were sampled during summer from coastal MA and in Monterey Bay, CA, and cells from both populations were dominated (> 70%) by haptophyte plastids of similar phylogenetic origin. L. viride were also evaluated from two freshwater ponds and possessed mostly Chrysochromulina sp. (haptophyte) and synurid (stramenopile) sequences. These results are the first survey of the genetic diversity of plastids associated with pelagic mixotrophic oligotrich ciliates and suggest that some species may selectively retain plastids from certain algal groups, while others appear to be generalists.

A decadal perspective on north water microbial eukaryotes as Arctic Ocean sentinels

“…Oligotrichia are often reported to be kleptoplastidic retaining chloroplasts from prey species to facilitate mixotrophy. In particular, the summer specialist Laboea (OTU-100) favors the retention of Micromonas chloroplasts and contributes to primary productivity in temperate seas 26 . It was also previously reported from summer North Water samples 17 and associated with longer day-length in the Beaufort Sea 27 , in keeping with it being a summer specialist.…”

The photic‐aphotic divide is a strong ecological and evolutionary force determining the distribution of ciliates (Alveolata, Ciliophora) in the ocean

“…The Oligotrichea also include mixoplankton species, of which we detected Pseudotontonia simplicidens (prevalent in the uppermost layers 0 and 1, above the DCM; Figure 3). Cells of P. simplicidens show chlorophyll a fluorescence and contain plastid 23S rRNA gene sequences, which suggest acquired photosynthetic capabilities (Johnson & Beaudoin, 2019; Pitta et al, 2000). Mixotrophy is a favored strategy in the upper, nutrient‐depleted waters in the Sargasso Sea (Blanco‐Bercial et al, 2022); combination of phagotrophy and photosynthesis would allow mixoplakton to escape from the nutrient limitation conditions (Edwards, 2019).…”

Changes in Ciliate Communities Reveal Modification of Lake Functioning Over the Last Century

“…As such, they can easily adapt to the more frequent exposure to extreme events or highly-variable environmental conditions that have occurred in lakes over the last decades 48 . Moreover, Limnostrombidium (synonym of Strombidium, from marine waters) is a common freshwater genus regrouping specialists mixotrophic species that preferentially feed and use the chloroplast of picophytoplankton 31,45,49 . Their signi cant increase in recent time thus indicates that recent changes in autotrophic picoplankton dynamic and structure, that have been previously recorded in some of our studied lakes 16 , might have provided them with a competitive advantage.…”