Abstract
Heterotrophic lineages of stramenopiles exhibit enormous diversity in morphology, lifestyle, and habitat. Among them, the marine stramenopiles (MASTs) represent numerous independent lineages that are only known from environmental sequences retrieved from marine samples. The core energy metabolism characterizing these unicellular eukaryotes is poorly understood. Here, we used single-cell genomics to retrieve, annotate, and compare the genomes of 15 MAST species, obtained by coassembling sequences from 140 individual cells sampled from the marine surface plankton. Functional annotations from their gene repertoires are compatible with all of them being phagocytotic. The unique presence of rhodopsin genes in MAST species, together with their widespread expression in oceanic waters, supports the idea that MASTs may be capable of using sunlight to thrive in the photic ocean. Additional subsets of genes used in phagocytosis, such as proton pumps for vacuole acidification and peptidases for prey digestion, did not reveal particular trends in MAST genomes as compared with nonphagocytotic stramenopiles, except a larger presence and diversity of V-PPase genes. Our analysis reflects the complexity of phagocytosis machinery in microbial eukaryotes, which contrasts with the well-defined set of genes for photosynthesis. These new genomic data provide the essential framework to study ecophysiology of uncultured species and to gain better understanding of the function of rhodopsins and related carotenoids in stramenopiles.
Highlights
Oceans are the largest habitats on Earth, and living biomass in these systems is dominated by planktonic microbes [1]
As comparative genomics suggested that the marine stramenopiles (MASTs) species investigated here were phagotrophs, we focused on genes putatively participating in the phagocytosis process
Genes clearly involved in phagocytosis, such as proton pumps for vacuole acidification and peptidases for prey digestion, were not exclusive of phagotrophic species and were represented in phototrophic and osmotrophic species
Summary
Oceans are the largest habitats on Earth, and living biomass in these systems is dominated by planktonic microbes [1]. We extended the dataset to 15 MAST species using SAGs from Tara Oceans and from other projects We investigated their trophic strategy using a comparative genomics model, and focused on a set of gene families relevant for phagocytosis. Microbial type I rhodopsins are photoactive proteins containing a retinal chromophore that work as light-driven proton pumps or photoreceptors [22, 23] They are widely present in marine microbes [24, 25] and have been found in MAST-4-C [26] and highly expressed in a growing MAST-4A population [27]. We have analyzed the genomes of 140 single cells retrieved during the Tara Oceans expedition as well as at the Blanes Bay Microbial Observatory (BBMO) These cells affiliate within seven MAST clades highly represented in marine molecular surveys [6]. We considered in detail the presence and diversity of proton pumps and microbial rhodopsins in MASTs to further understand the potential physiological cell capabilities and the role of light in phagolysosome acidification
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