Inheritance of spheroid body and plastid in the raphid diatom <i>Epithemia</i> (Bacillariophyta) during sexual reproduction

Kamakura, Shiho; Mann, David G.; Nakamura, Noriaki; Sato, Shinya

doi:10.1080/00318884.2021.1909399

Cited by 5 publications

(13 citation statements)

References 61 publications

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“…The cleaned frustules were subsequently placed on a coverslip (3 mm diameter; Matsunami Glass Ind., Osaka, Japan), coated with osmium oxide (OsO 4 ) using an ion sputter NEOC-AN (Meiwafosis, Tokyo, Japan) and observed using an S-5000 SEM (Hitachi, Tokyo, Japan). To support our identification, we previously performed phylogenetic analysis with 18S rDNA (Kamakura and Sato 2018), showing that the strains of our E. gibba var. ventricosa and Epithemia sp.…”

Section: Observationsmentioning

confidence: 74%

“…Based on field observations of the seasonality of auxosporulation and culture experiments, sexual reproduction of pennate diatoms could likely be controlled by light conditions and temperature (Chepurnov et al 2004;Mouget et al 2009). Sexual reproduction in Epithemia, including taxa formerly classified under Rhopalodia, has been documented previously (Thwaites 1847;Smith 1853;Klebahn 1896;Karsten 1899;Geitler 1932Geitler , 1977Kamakura et al 2021). This genus recovers cell sizes through heterothallic reproduction, whereas homothallism and automixis have not been observed.…”

Section: Life Cycles Of Two Epithemia Taxamentioning

confidence: 96%

“…Initial cells of E. gibba var. ventricosa formed via sexual reproduction are 105-185 μm (Kamakura et al 2021). We regard cells within this size range as potential initial cells, providing indirect evidence of sexual reproduction at our sampling site.…”

Section: Valve Length Of Cells In the Field Samplesmentioning

confidence: 99%

“…Our Epithemia sp. has been sporadically reported from Japan and historically referred to as Rhopalodia acuminata Krammer (Kihara et al 2009(Kihara et al , 2015, R. michelorum Krammer (Ohtsuka 2002;Takano et al 2009;Kamakura and Sato 2018;Sato et al 2020) and R. gibberula var. vanheurckii Müller (Ohtsuka and Kitano 2020).…”

Section: Taxonomic Implicationsmentioning

confidence: 99%

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Differential cell size reduction of two sympatric Epithemia (Bacillariophyta) taxa in Nakaikemi Wetland, Japan

Kamakura,

Ohtsuka,

Nagumo

et al. 2024

Phycological Research

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SUMMARYWe observed contrasting temporal changes in cell size between two Epithemia taxa. The life cycle of diatoms is closely linked to their cell size, with a gradual decrease during the vegetative stage and a recovery through sexual reproduction. Sexual reproduction is triggered when cells become smaller than a species‐specific size threshold and receive species‐specific environmental cues. Few studies have documented the life cycles and frequency of sexual reproduction in diatoms, combining field observations and laboratory culture. We collected two Epithemia taxa, Epithemia gibba var. ventricosa and Epithemia sp. from a pond in Nakaikemi Wetland, and measured their valve lengths monthly for almost 3 years. Additionally, we established cultures of both taxa to examine the rates of cell size reduction, which affect the duration of the vegetative stage. In the field, E. gibba var. ventricosa exhibited a wide range of cell sizes and signs of size recovery. Furthermore, the cultures of this taxon showed a clear decrease in cell size through division, suggesting that sexual reproduction is required for size recovery. On the other hand, Epithemia sp. showed no obvious change in cell size both in the field and in the laboratory. This suggests that either sexual reproduction is not necessary for this taxon to maintain its population or their life cycle extends over several years to several decades. Thus, our findings reveal congeneric taxa sharing a common habitat and substratum, yet exhibiting distinct sexual and asexual strategies. Furthermore, we question the validity of taxonomic classifications previously assigned to these diatoms based on the range of morphological characteristics observed in the present study.

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Section: Observationsmentioning

confidence: 74%

Section: Life Cycles Of Two Epithemia Taxamentioning

confidence: 96%

Section: Valve Length Of Cells In the Field Samplesmentioning

confidence: 99%

Section: Taxonomic Implicationsmentioning

confidence: 99%

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Differential cell size reduction of two sympatric Epithemia (Bacillariophyta) taxa in Nakaikemi Wetland, Japan

Kamakura,

Ohtsuka,

Nagumo

et al. 2024

Phycological Research

Self Cite

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show abstract

“…Consistent with their being obligate endosymbionts, diazoplasts have never been observed outside their diatom, and isolated diazoplasts cannot be grown in laboratory cultures outside the host cells. Diazoplasts are not only vertically transmitted during cell division but show uniparental inheritance during sexual reproduction, demonstrating robust mechanisms for inheritance of the diazoplast (20). Although Epithemia spp.…”

Section: Introductionmentioning

confidence: 99%

The endosymbiont ofEpithemia clementinais specialized for nitrogen fixation within a photosynthetic eukaryote

Moulin

Frail

Braukmann

et al. 2023

Preprint

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Nitrogen is a limiting nutrient for photosynthetic productivity. Yet biological nitrogen fixation which transforms abundant atmospheric nitrogen to bioavailable ammonia is largely restricted to bacteria. Epithemia spp. diatoms contain obligate, nitrogen-fixing endosymbionts, or 'diazoplasts', derived from cyanobacteria. They represent rare photosynthetic eukaryotes that have successfully coupled oxygenic photosynthesis with oxygen-sensitive nitrogenase activity. Here, we report a newly-isolated species, E. clementina, as a model to investigate endosymbiotic acquisition of this critical biological function. To detect the metabolic changes associated with endosymbiotic specialization, we compared nitrogen fixation, nitrogen utilization, and their regulatory pathways in the Epithemia diazoplast with its close free-living cyanobacteria relative, Crocosphaera subtropica. Unlike C. subtropica, we show that nitrogenase activity in the diazoplast is concurrent with, and even dependent on, host photosynthesis. In contrast to its expanded nitrogen-fixing activity, the diazoplast has diminished ability to utilize alternative nitrogen sources. Finally, while key regulators of nitrogen metabolism are retained in the diazoplast genome, we observed a conserved negative feedback regulation of nitrogen fixation to ammonium, but paradoxical nitrogen assimilation responses in the diazoplast compared with C. subtropica. Our results suggest key adaptations that facilitated the transition from free-living to endosymbiotic specialist diazotroph, including import of host carbohydrates, streamlined carbon catabolism favoring high respiratory rates, and altered nitrogen regulation to favor nitrogen transfer to the host. Elucidating how photosynthesis and nitrogen fixation are coupled in a eukaryotic cell has important implications for bioengineering nitrogen-fixing crop plants for sustainable agriculture.

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The endosymbiont of Epithemia clementina is specialized for nitrogen fixation within a photosynthetic eukaryote

Moulin,

Frail,

Braukmann

et al. 2024

ISME Communications

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Epithemia spp. diatoms contain obligate, nitrogen-fixing endosymbionts, or diazoplasts, derived from cyanobacteria. These algae are a rare example of photosynthetic eukaryotes that have successfully coupled oxygenic photosynthesis with oxygen-sensitive nitrogenase activity. Here, we report a newly-isolated species, E. clementina, as a model to investigate endosymbiotic acquisition of nitrogen fixation. We demonstrate that the diazoplast, which has lost photosynthesis, provides fixed nitrogen to the diatom host in exchange for fixed carbon. To identify the metabolic changes associated with this endosymbiotic specialization, we compared the Epithemia diazoplast with its close, free-living cyanobacterial relative, Crocosphaera subtropica. Unlike C. subtropica, in which nitrogenase activity is temporally separated from photosynthesis, we show that nitrogenase activity in the diazoplast is continuous through the day (concurrent with host photosynthesis) and night. Host and diazoplast metabolism are tightly coupled to support nitrogenase activity: Inhibition of photosynthesis abolishes daytime nitrogenase activity, while nighttime nitrogenase activity no longer requires cyanobacterial glycogen storage pathways. Instead, import of host-derived carbohydrates supports nitrogenase activity throughout the day-night cycle. Carbohydrate metabolism is streamlined in the diazoplast compared to C. subtropica with retention of the oxidative pentose pathway and oxidative phosphorylation. Similar to heterocysts, these pathways may be optimized to support nitrogenase activity, providing reducing equivalents and ATP and consuming oxygen. Our results demonstrate that the diazoplast is specialized for endosymbiotic nitrogen fixation. Altogether, we establish a new model for studying endosymbiosis, perform a functional characterization of this diazotroph endosymbiosis, and identify metabolic adaptations for endosymbiotic acquisition of a critical biological function.

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Inheritance of spheroid body and plastid in the raphid diatom Epithemia (Bacillariophyta) during sexual reproduction

Abstract: Inheritance of spheroid body and plastid in the raphid diatom Epithemia (Bacillariophyta) during sexual reproduction". Phycologia 60 (3). 265-273. Taylor and Francis.

Cited by 5 publications

References 61 publications

Differential cell size reduction of two sympatric Epithemia (Bacillariophyta) taxa in Nakaikemi Wetland, Japan

Differential cell size reduction of two sympatric Epithemia (Bacillariophyta) taxa in Nakaikemi Wetland, Japan

The endosymbiont ofEpithemia clementinais specialized for nitrogen fixation within a photosynthetic eukaryote

The endosymbiont of Epithemia clementina is specialized for nitrogen fixation within a photosynthetic eukaryote

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