Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs

Ban, Hiroki; Sato, Shinya; Yamada, Kazumasa; Nakamura, Yoji; Ichinomiya, Mutsuo; Sato, Naoki; Blanc-Mathieu, Romain; Endo, Hisashi; Kuwata, Akira; Ogata, Hiroyuki

doi:10.1038/s42003-023-05002-x

Cited by 4 publications

(20 citation statements)

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“…We collected full-length parmalean 18S rRNA genes from the SILVA database (categorized as “Bolidomonas”; accessed Jun 2023) (Quast et al, 2012) and from published work (Ban et al, 2023). We added some diatom sequences as outgroups to the dataset and then removed previously reported chimeric sequences (Ichinomiya et al, 2016) and sequences shorter than 900 bp.…”

Section: Methodsmentioning

confidence: 99%

“…Consequently, the order Parmales was re-established under the class Bolidophyceae (Ichinomiya et al, 2016). The two forms have a phylogenetically nested relationship, and the silicified strains possess the genomic potential to form flagella, suggesting that these two forms represent different stages in the life cycle of the same organisms (Ichinomiya et al, 2016; Yamada et al, 2020; Ban et al, 2023). Currently, there are four identified morphotypes of silicified parmaleans, each distinguished by the morphological features of their silicified cell walls: Triparma , Tetraparma , ‘Scaly parma’, and Pentalamina , of which the last morphotype has not yet been isolated (Booth and Marchant, 1987; Ban et al, 2023; Sato et al, Unpublished).…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

“…Their life cycle and predicted phago-mixotrophic nutrient acquisition contrast sharply with those of diatoms, their closest evolutionary photo-autotrophic relatives (Ban et al, 2023). Therefore, Parmales is a key eukaryotic group in understanding the physiology, ecology, and evolution of diatoms, the most successful phytoplankton group in the modern ocean (Kuwata et al, 2018; Ban et al, 2023). In particular, characterizing the diversity and biogeography of Parmales across space and niches is expected to provide fundamental information on the difference in the ecological and evolutionary strategies between diatoms and Parmales.…”

Section: Introductionmentioning

confidence: 99%

“…In this study, we use the EukBank database, which provides by far the largest dataset for DNA metabarcodes targeting the 18S rRNA gene V4 region (Kaneko et al, 2023), and associate these data with the current knowledge of Parmales, including information from recent isolates from Triparma , Tetraparma , and ‘Scaly parma’ (Yamada et al, 2020; Ban et al, 2023). The EukBank project consolidates multiple datasets originating from various sampling projects including Tara Oceans (Pesant et al, 2015; Sunagawa et al, 2020), Malaspina (Logares et al, 2020), and Australian Microbiome (Brown et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Global distribution and diversity of marine Parmales

Ban,

Endo,

Kuwata

et al. 2023

Preprint

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Parmales (Bolidophyceae) is a minor eukaryotic phytoplankton group, sister to diatoms, that exists as two distinct forms of unicellular organisms: silicified cells and naked flagellates. Since their discovery, many field studies of Parmales have been performed, but their global distribution remains under-investigated. Here, we compile over 3,000 marine DNA metabarcoding datasets targeting the V4 region of the 18S rRNA gene from the EukBank database. By linking this large dataset with the latest morphological and genetic information, we provide updated estimates on the diversity and distribution of Parmales in the global ocean at a fine taxonomic resolution. Parmalean amplicon sequence variants (ASVs) were detected in nearly 90% of the analyzed samples. However, the relative abundance of parmaleans in the eukaryotic community is less than 0.2% on average, and the estimated true richness of parmalean ASVs is about 316 ASVs, confirming their low abundance and low diversity. Phylogenetic analysis clearly divides these algae into four clades, and three known morphotypes of silicified cells were classified into three different clades. The abundance of Parmales is generally high in the pole and decreases toward the tropics, and individual clades/subclades show further distinctions in distributions. Overall, our results suggest their clade/subclade-specific adaptation to different ecological niches.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Global distribution and diversity of marine Parmales

Ban,

Endo,

Kuwata

et al. 2023

Preprint

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Integrated overview of stramenopile ecology, taxonomy, and heterotrophic origin

Jirsová,

Wideman

2024

The ISME Journal

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Stramenopiles represent a significant proportion of aquatic and terrestrial biota. Most biologists can name a few, but these are limited to the phototrophic (e.g., diatoms and kelp) or parasitic species (e.g., oomycetes, Blastocystis), with free-living heterotrophs largely overlooked. Though our attention is slowly turning towards heterotrophs, we have only a limited understanding of their biology due to a lack of cultured models. Recent metagenomic and single-cell investigations have revealed the species richness and ecological importance of stramenopiles—especially heterotrophs. However, our lack of knowledge of the cell biology and behaviour of these organisms leads to our inability to match species to their particular ecological functions. Because photosynthetic stramenopiles are studied independently of their heterotrophic relatives, they are often treated separately in the literature. Here, we present stramenopiles as a unified group with shared synapomorphies and evolutionary history. We introduce the main lineages, describe their important biological and ecological traits, and provide a concise update on the origin of the ochrophyte plastid. We highlight the crucial role of heterotrophs and mixotrophs in our understanding of stramenopiles with the goal of inspiring future investigations in taxonomy and life history. To understand each of the many diversifications within stramenopiles—towards autotrophy, osmotrophy, or parasitism—we must understand the ancestral heterotrophic flagellate from which they each evolved. We hope the following will serve as a primer for new stramenopile researchers or as an integrative refresher to those already in the field.

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Multiple plastid losses within photosynthetic stramenopiles revealed by comprehensive phylogenomics

Terpis,

Salomaki,

Barcytė

et al. 2024

Preprint

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Ochrophyta is a vast and morphologically diverse group of algae with complex plastids, including familiar taxa with fundamental ecological importance (diatoms or kelp), and a wealth of lesser-known and obscure organisms. The sheer diversity of ochrophytes poses a challenge for reconstructing their phylogeny, with major gaps in sampling and an unsettled placement of particular taxa yet to be tackled. We sequenced transcriptomes from 25 strategically selected representatives and used these data to build the most taxonomically comprehensive ochrophyte-centered phylogenomic supermatrix to date. We employed a combination of approaches to reconstruct and critically evaluate the relationships among ochrophytes. While generally congruent with previous analyses, the updated ochrophyte phylogenomic tree resolved the position of several taxa with previously uncertain placement, and supported a redefinition of the class Synchromophyceae. Our results indicated that the heterotrophic plastid-lacking heliozoanActinophrys solis not a sister lineage of ochrophytes, as proposed recently, but rather phylogenetically nested among them. In addition, we foundPicophagus flagellatusto be a secondarily heterotrophic ochrophyte lacking all hallmark plastid genes, yet exhibiting mitochondrial proteins that seem to be genetic footprints of lost plastid organelle. We thus document, for the first time, plastid loss in two separate ochrophyte lineages. Altogether, our study provides a new framework for reconstructing trait evolution in ochrophytes and demonstrates that plastid loss is more common than previously thought.Issue Section:Discoveries

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Genome analysis of Parmales, the sister group of diatoms, reveals the evolutionary specialization of diatoms from phago-mixotrophs to photoautotrophs

Cited by 4 publications

References 133 publications

Global distribution and diversity of marine Parmales

Global distribution and diversity of marine Parmales

Integrated overview of stramenopile ecology, taxonomy, and heterotrophic origin

Multiple plastid losses within photosynthetic stramenopiles revealed by comprehensive phylogenomics

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