A single loss of photosynthesis in the diatom order Bacillariales (Bacillariophyta)

Onyshchenko, Anastasiia; Ruck, Elizabeth C.; Nakov, Teofil; Alverson, Andrew J.

doi:10.1002/ajb2.1267

Cited by 17 publications

(30 citation statements)

References 71 publications

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“…Nitzschia Nitz4 grew well in near-axenic culture for approximately one year before dying due to size diminution after failing to reproduce sexually. Although we were not able to assign a name to this species, phylogenetic analyses placed it within a clade composed exclusively of nonphotosynthetic Nitzschia [20].…”

Section: Resultsmentioning

confidence: 76%

“…To understand the genomic signatures of the transition from mixotrophy to heterotrophy, we collected and isolated nonphotosynthetic Nitzschia [20] from a locale known to harbor several species [27]. We generated an annotated genome for one strain, Nitzschia sp.…”

Section: Resultsmentioning

confidence: 99%

“…We examined the fully sequenced plastid genomes of Nitzschia Nitz4 [20] and another apochloritic Nitzschia [NIES-3581; 22] to understand how loss of photosynthesis impacted the plastid genome. Both plastid genomes revealed a substantial reduction in the amount of intergenic DNA and wholesale loss of genes encoding the photosynthetic apparatus, including those involved in carbon fixation, photosystems I and II, the cytochrome b6f complex, and porphyrin and thiamine metabolism (Table 1).…”

Section: Plastid Genome Reductionmentioning

confidence: 99%

“…The plastid genome also experienced a substantial downward shift in GC content, from >30% in photosynthetic species to just 22.4% in Nitzschia Nitz4 (Table 1), a pattern that is common in streamlined bacterial genomes [29] and may reflect mutational bias [30] or nitrogen frugality [GC base pairs contain more nitrogen than AT base pairs; 31]. Oudot-Le Secq et al [32] Zheng et al [33] Crowell et al [34] Onyshchenko et al [20] 1 Gene count includes rRNAs, tRNAs, and ORFs of unknown function.…”

Section: Plastid Genome Reductionmentioning

confidence: 99%

“…Like many plant and algal lineages that are ancestrally and predominantly photoautotrophic, some diatoms have completely lost their ability to photosynthesize and are obligate heterotrophs, relying exclusively on extracellular carbon for growth [11]. Unlike some species-rich lineages of photoautotrophs, such as flowering plants and red algae that have lost photosynthesis many times [18,19], loss of photosynthesis has occurred rarely in diatoms, with just two known losses that have spawned a small number (≈ 20) of species [20,21]. These so-called "apochloritic" diatoms maintain colorless plastids with highly reduced, AT-rich plastid genomes that are devoid of photosynthesis-related genes [20,22].…”

Section: Introductionmentioning

confidence: 99%

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The genome of a nonphotosynthetic diatom provides insights into the metabolic shift to heterotrophy and constraints on the loss of photosynthesis

Pendergrass

Roberts

Ruck

et al. 2020

Preprint

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AbstractAlthough most of the tens of thousands of diatom species are obligate photoautotrophs, many mixotrophic species can also use extracellular organic carbon for growth, and a small number of obligate heterotrophs have lost photosynthesis entirely. We sequenced the genome of a nonphotosynthetic diatom, Nitzschia sp. strain Nitz4, to determine how carbon metabolism was altered in the wake of this rare and radical trophic shift in diatoms. Like other groups that have lost photosynthesis, the genomic consequences were most evident in the plastid genome, which is exceptionally AT-rich and missing photosynthesis-related genes. The relatively small (27 Mb) nuclear genome did not differ dramatically from photosynthetic diatoms in gene or intron density. Genome-based models suggest that central carbon metabolism, including a central role for the plastid, remains relatively intact in the absence of photosynthesis. All diatom plastids lack an oxidative pentose phosphate pathway (PPP), leaving photosynthesis as the main source of plastid NADPH. Consequently, nonphotosynthetic diatoms lack the primary source of NADPH required for essential biosynthetic pathways that remain in the plastid. Genomic models highlighted similarities between nonphotosynthetic diatoms and apicomplexan parasites for provisioning NADPH in their plastids. The ancestral absence of a plastid PPP might constrain loss of photosynthesis in diatoms compared to Archaeplastida, whose plastid PPP continues to produce reducing cofactors following loss of photosynthesis. Finally, Nitzschia possesses a complete β-ketoadipate pathway. Previously known only from fungi and bacteria, this pathway may allow mixotrophic and heterotrophic diatoms to obtain energy through the degradation of abundant plant-derived aromatic compounds.

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Section: Resultsmentioning

confidence: 76%

Section: Resultsmentioning

confidence: 99%

Section: Plastid Genome Reductionmentioning

confidence: 99%

Section: Plastid Genome Reductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

The genome of a nonphotosynthetic diatom provides insights into the metabolic shift to heterotrophy and constraints on the loss of photosynthesis

Pendergrass

Roberts

Ruck

et al. 2020

Preprint

Self Cite

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show abstract

Constraint-Based Modeling of Diatoms Metabolism and Quantitative Biology Approaches

Kumar

Zuñiga

Tibocha‐Bonilla

et al. 2022

The Molecular Life of Diatoms

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Reconstructing Dynamic Evolutionary Events in Diatom Nuclear and Organelle Genomes

Dorrell

Liu

Bowler

2022

The Molecular Life of Diatoms

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The diatoms evolved within the stramenopiles, an ecologically important and diverse assemblage of eukaryotes that includes both photosynthetic macrophytes and microalgae, as well as non-photosynthetic heterotrophs and parasites. The evolutionary history of the stramenopiles, which stretches back to the Palaeozoic, has been marked by the acquisition of chloroplasts in a recent common ancestor of their photosynthetic members, the ochrophytes; and progressive gains of genes in the nuclear genome by horizontal and endosymbiotic gene transfer. Here, we place diatoms in their actual evolutionary context within the stramenopiles; identify gene transfers that have shaped the coding content of the diatom nucleus; and profile sources of differences in chloroplast and mitochondrial genome content between different stramenopiles including diatoms. We underline the importance of considering diatoms as evolutionary mosaics, supported by genes of bacterial, red, green and other eukaryotic algal origin as illustrated by multiple phylogenomic studies realised over the last two decades; and the relatively limited changes to organelle genome content in diatoms compared to other stramenopile lineages. However, we identify a previously undocumented transfer of a novel open reading frame of the chloroplasts of green algae into the ochrophytes, underlining the importance of changes in organelle and nuclear gene content, in defining the current biology of diatoms.

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A single loss of photosynthesis in the diatom order Bacillariales (Bacillariophyta)

Cited by 17 publications

References 71 publications

The genome of a nonphotosynthetic diatom provides insights into the metabolic shift to heterotrophy and constraints on the loss of photosynthesis

The genome of a nonphotosynthetic diatom provides insights into the metabolic shift to heterotrophy and constraints on the loss of photosynthesis

Constraint-Based Modeling of Diatoms Metabolism and Quantitative Biology Approaches

Reconstructing Dynamic Evolutionary Events in Diatom Nuclear and Organelle Genomes

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