Diel-Regulated Transcriptional Cascades of Microbial Eukaryotes in the North Pacific Subtropical Gyre.

Ryan D Groussman,Bryndan P Durham,Sacha N Coesel,E Virginia Armbrust

doi:10.3389/fmicb.2021.682651

Ryan D Groussman, Bryndan P Durham + Show 2 more

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https://doi.org/10.3389/fmicb.2021.682651

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Abstract

Open-ocean surface waters host a diverse community of single-celled eukaryotic plankton (protists) consisting of phototrophs, heterotrophs, and mixotrophs. The productivity and biomass of these organisms oscillate over diel cycles, and yet the underlying transcriptional processes are known for few members of the community. Here, we examined a 4-day diel time series of transcriptional abundance profiles for the protist community (0.2–100 μm in cell size) in the North Pacific Subtropical Gyre near Station ALOHA. De novo assembly of poly-A+ selected metatranscriptomes yielded over 30 million contigs with taxonomic and functional annotations assigned to 54 and 25% of translated contigs, respectively. The completeness of the resulting environmental eukaryotic taxonomic bins was assessed, and 48 genera were further evaluated for diel patterns in transcript abundances. These environmental transcriptome bins maintained reproducible temporal partitioning of total gene family abundances, with haptophyte and ochrophyte genera generally showing the greatest diel partitioning of their transcriptomes. The haptophyte Phaeocystis demonstrated the highest proportion of transcript diel periodicity, while most other protists had intermediate levels of periodicity regardless of their trophic status. Dinoflagellates, except for the parasitoid genus Amoebophrya, exhibit the fewest diel oscillations of transcript abundances. Diel-regulated gene families were enriched in key metabolic pathways; photosynthesis, carbon fixation, and fatty acid biosynthesis gene families had peak times concentrated around dawn, while gene families involved in protein turnover (proteasome and protein processing) are most active during the high intensity daylight hours. TCA cycle, oxidative phosphorylation and fatty acid degradation predominantly peaked near dusk. We identified temporal pathway enrichments unique to certain taxa, including assimilatory sulfate reduction at dawn in dictyophytes and signaling pathways at early evening in haptophytes, pointing to possible taxon-specific channels of carbon and nutrients through the microbial community. These results illustrate the synchrony of transcriptional regulation to the diel cycle and how the protist community of the North Pacific Subtropical Gyre structures their transcriptomes to guide the daily flux of matter and energy through the gyre ecosystem.

Highlights

The North Pacific Subtropical Gyre (NPSG) is a warm and oligotrophic ecosystem that hosts a diverse community of phototrophic, heterotrophic, and mixotrophic microbial eukaryotes spanning over three orders of magnitude in cell sizes
Phototrophic members of the NPSG eukaryotic phytoplankton consist of haptophytes including Emiliania huxleyi (Hernández et al, 2020) and diatoms such as Rhizosolenia and Hemiaulus (Villareal et al, 1993), two genera found in symbioses with nitrogen fixing cyanobacteria that bloom during sporadic injections of nutrients into the surface waters
We examined the transcriptional profiles of eukaryotic microbes over the diel cycle by collecting size-fractionated (0.2–100 μm) RNA samples every 4 h over 4 consecutive days in the oligotrophic North Pacific Subtropical Gyre (NPSG), ∼100 km NE of Station ALOHA

Summary

Introduction

The North Pacific Subtropical Gyre (NPSG) is a warm and oligotrophic (nitrogen-limited) ecosystem that hosts a diverse community of phototrophic, heterotrophic, and mixotrophic microbial eukaryotes (protists) spanning over three orders of magnitude in cell sizes. Ochrophyte, and dinoflagellate lineages are constitutive mixotrophs (Faure et al, 2019), with evidence that they can graze on picocyanobacteria in the NPSG (Frias-Lopez et al, 2009). In the well-lit and low nutrient conditions of the NPSG, mixotrophy may be advantageous (Rothhaupt, 1996), and the gene family abundance profiles of many environmental protist species suggest widespread mixotrophy (Lambert et al, 2021). Some ciliates, such as Strombidium, are non-constitutive mixotrophs that retain the plastid of their consumed prey (Stoecker et al, 2009; Faure et al, 2019)

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