Comparative Plastid Genomics of Non-Photosynthetic Chrysophytes: Genome Reduction and Compaction

Abstract

Spumella-like heterotrophic chrysophytes are important eukaryotic microorganisms that feed on bacteria in aquatic and soil environments. They are characterized by their lack of pigmentation, naked cell surface, and extremely small size. Although Spumella-like chrysophytes have lost their photosynthetic ability, they still possess a leucoplast and retain a plastid genome. We have sequenced the plastid genomes of three nonphotosynthetic chrysophytes, Spumella sp. Baeckdong012018B8, Pedospumella sp. Jangsampo120217C5 and Poteriospumella lacustris Yongseonkyo072317C3, and compared them to the previously sequenced plastid genome of "Spumella" sp. NIES-1846 and photosynthetic chrysophytes. We found the plastid genomes of Spumella-like flagellates to be generally conserved with respect to genome structure and housekeeping gene content. We nevertheless also observed lineage-specific gene rearrangements and duplication of partial gene fragments at the boundary of the inverted repeat and single copy regions. Most gene losses correspond to genes for proteins involved in photosynthesis and carbon fixation, except in the case of petF. The newly sequenced plastid genomes range from~55.7 kbp to~62.9 kbp in size and share a core set of 45 protein-coding genes, 3 rRNAs, and 32 to 34 tRNAs. Our results provide insight into the evolutionary history of organelle genomes via genome reduction and gene loss related to loss of photosynthesis in chrysophyte evolution.

A cryptic plastid and a novel mitochondrial plasmid inLeucomyxa plasmidiferagen. and sp. nov. (Ochrophyta) push the frontiers of organellar biology

“…To this end we constructed a supermatrix of 30 plastid genome-encoded proteins, sampling selected ochrophytes (to have represented all classes with plastid genome data available) and several non-ochrophyte algae as an outgroups. Analyses of the data (6,627 aligned amino acid positions) using the maximum likelihood method and the complex model LG+C60+F+G yielded a tree topology (figure 5) that is generally congruent with recent phylogenetic analyses based on multiple plastid genome-encoded proteins (Ševčíková et al 2019;Han et al 2019;Kim et al 2020;Barcytė et al 2021;Di Franco et al 2022). However, thanks to new plastid genome data that became available only recently, our tree is more comprehensive in terms of the main lineages of ochrophytes represented, and exhibits several notable features.…”

“…The L. salinum also apparently lacks ferredoxin-NADP + reductase and ferredoxin, the latter being a functionally versatile protein with a redox-active iron-sulfur (Fe-S) cluster and involved in multiple plastid-localized processes beyond photosynthesis itself (Hanke and Mulo 2013). This is even more notable considering the fact that a ferredoxin-encoding gene ( petF ) has been retained by plastid genomes of several independently evolved non-photosynthetic chrysophytes (Dorrell et al 2019; Kim et al 2020). Related to this is the absence in L. salinum of all components of the SUF system, a plastid-specific machinery for the assembly of Fe-S clusters.…”

Molecular Phylogeny and Taxonomy of the Genus Spumella (Chrysophyceae) Based on Morphological and Molecular Evidence

“…However, the recently described genera Poteriospumella and Cornospumella do not show clear ultrastructural evidence, with the leucoplast not appearing to be encircled by the nuclear outer membrane ( Grossmann et al, 2016 ). According to genomic and transcriptomic studies ( Beisser et al, 2017 ; Graupner et al, 2018 ; Olefeld et al, 2018 ; Dorrell et al, 2019 ; Kim et al, 2020 ), the leucoplast of non-photosynthetic Chrysophyceae was found to have a reduced plastid genome. The plastid genome and transcriptome data showed that the non-photosynthetic lineages of chrysophytes lost most of their photosynthesis-related genes and evolved from phototrophic lineages.…”

“…Spumella- like flagellates are non-photosynthetic unicellular organisms with two unequal flagella that have a simple morphology, e.g., spherical or naked cells ( Cienkowsky, 1870 ; Berglund et al, 2005 ; Boenigk et al, 2005 ; Lepère et al, 2006 ; Charvet et al, 2012 ). They are representative heterotrophic chrysophytes that underwent independent loss of photosynthetic ability in the chrysophyte lineage ( Boenigk et al, 2005 ; Boenigk, 2008 ; Grossmann et al, 2016 ; Kim et al, 2020 ). As they are one of the major bacterivore groups in aquatic systems, their significance in carbon transfer from the microbial loop has been emphasized ( Wylie and Currie, 1991 ; Sanders et al, 1994 ; Sherr and Sherr, 1994 ; Arndt et al, 2000 ; Boenigk and Arndt, 2002 ).…”

“…The genus Spumella is characterized by small cells (≤10 μm) with a spherical, sometimes elongated oval or oboval shape and a naked surface, two unequal flagella and colorlessness. Members of the genus lost their photosynthetic ability but still have a vestigial plastid ( Preisig and Hibberd, 1983 ; Mylnikov et al, 2008 ; Grossmann et al, 2016 ) and retained their plastid genome ( Beisser et al, 2017 ; Graupner et al, 2018 ; Dorrell et al, 2019 ; Kim et al, 2020 ). In particular, Spumella vivipara Kent, S. sphaerophora (Skuja) Mignot and S. mior (Skuja) Zhukov have strikingly large cell sizes of approximately 20 μm ( Kent, 1880 ; Skuja, 1956 ; Mignot, 1977 ; Mylnikov and Mylnikova, 2005 ).…”