Serial Gene Losses and Foreign DNA Underlie Size and Sequence Variation in the Plastid Genomes of Diatoms

Ruck, Elizabeth C.; Nakov, Teofil; Jansen, Robert K.; Theriot, Edward C.; Alverson, Andrew J.

doi:10.1093/gbe/evu039

Cited by 65 publications

(103 citation statements)

References 67 publications

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“…In contrast, genome organization of outgroup species varies considerably. The Thalassiosirales show a much higher level of conservation of genome organization compared to a recent comparison of a more phylogenetically diverse assemblage of diatoms [16]. Denser sampling of this order provides valuable insights into the dynamics of plastid genome evolution within a single order.…”

Section: Discussionmentioning

confidence: 93%

Conserved Gene Order and Expanded Inverted Repeats Characterize Plastid Genomes of Thalassiosirales

Sabir

Ashworth

et al. 2014

PLoS ONE

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Diatoms are mostly photosynthetic eukaryotes within the heterokont lineage. Variable plastid genome sizes and extensive genome rearrangements have been observed across the diatom phylogeny, but little is known about plastid genome evolution within order- or family-level clades. The Thalassiosirales is one of the more comprehensively studied orders in terms of both genetics and morphology. Seven complete diatom plastid genomes are reported here including four Thalassiosirales: Thalassiosira weissflogii, Roundia cardiophora, Cyclotella sp. WC03_2, Cyclotella sp. L04_2, and three additional non-Thalassiosirales species Chaetoceros simplex, Cerataulina daemon, and Rhizosolenia imbricata. The sizes of the seven genomes vary from 116,459 to 129,498 bp, and their genomes are compact and lack introns. The larger size of the plastid genomes of Thalassiosirales compared to other diatoms is due primarily to expansion of the inverted repeat. Gene content within Thalassiosirales is more conserved compared to other diatom lineages. Gene order within Thalassiosirales is highly conserved except for the extensive genome rearrangement in Thalassiosira oceanica. Cyclotella nana, Thalassiosira weissflogii and Roundia cardiophora share an identical gene order, which is inferred to be the ancestral order for the Thalassiosirales, differing from that of the other two Cyclotella species by a single inversion. The genes ilvB and ilvH are missing in all six diatom plastid genomes except for Cerataulina daemon, suggesting an independent gain of these genes in this species. The acpP1 gene is missing in all Thalassiosirales, suggesting that its loss may be a synapomorphy for the order and this gene may have been functionally transferred to the nucleus. Three genes involved in photosynthesis, psaE, psaI, psaM, are missing in Rhizosolenia imbricata, which represents the first documented instance of the loss of photosynthetic genes in diatom plastid genomes.

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Section: Discussionmentioning

confidence: 93%

Conserved Gene Order and Expanded Inverted Repeats Characterize Plastid Genomes of Thalassiosirales

Sabir

Ashworth

et al. 2014

PLoS ONE

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“…Until recently, it was thought that plastids were impenetrable to foreign DNA (85,86). However, new data from various angiosperms uncovered mitochondrion-to-plastid (87,88) and nucleusto-plastid DNA migration events (89), and there are also examples of plastids, including those of some diatoms and the red alga Gracilaria tenuistipitata, acquiring genes from plasmid or bacterial genomes (69,90). Foreign DNA can also come in the form of extrachromosomal elements.…”

Section: A Multiplicity Of Mitochondrial and Plastid Genome Architectmentioning

confidence: 99%

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

Smith

Keeling

2015

Proc. Natl. Acad. Sci. U.S.A.

355

344

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Mitochondrial and plastid genomes show a wide array of architectures, varying immensely in size, structure, and content. Some organelle DNAs have even developed elaborate eccentricities, such as scrambled coding regions, nonstandard genetic codes, and convoluted modes of posttranscriptional modification and editing. Here, we compare and contrast the breadth of genomic complexity between mitochondrial and plastid chromosomes. Both organelle genomes have independently evolved many of the same features and taken on similar genomic embellishments, often within the same species or lineage. This trend is most likely because the nuclear-encoded proteins mediating these processes eventually leak from one organelle into the other, leading to a high likelihood of processes appearing in both compartments in parallel. However, the complexity and intensity of genomic embellishments are consistently more pronounced for mitochondria than for plastids, even when they are found in both compartments. We explore the evolutionary forces responsible for these patterns and argue that organelle DNA repair processes, mutation rates, and population genetic landscapes are all important factors leading to the observed convergence and divergence in organelle genome architecture.E ndosymbiosis can dramatically impact cellular and genomic architectures. Mitochondria and plastids exemplify this point. Each of these two types of energy-producing eukaryotic organelle independently arose from the endosymbiosis, retention, and integration of a free-living bacterium into a host cell more than 1.4 billion years ago. Mitochondria came first, evolving from an alphaproteobacterial endosymbiont in an ancestor of all known living eukaryotes, and still exist, in one form or another (1), in all its descendants (2). Plastids came later, via the "primary" endosymbiosis of a cyanobacterium by the eukaryotic ancestor of the Archaeplastida, and then spread laterally to disparate groups through eukaryote-eukaryote endosymbioses (3). Consequently, a significant proportion of the identified eukaryotic diversity has a plastid.With few exceptions (1, 4), mitochondria and plastids contain genomes-chromosomal relics of the bacterial endosymbionts from which they evolved (2, 5). Mitochondrial and plastid DNAs (mtDNAs and ptDNAs) have many traits in common, which is not surprising given their similar evolutionary histories. Both are highly reduced relative to the genomes of extant, free-living alphaproteobacteria and cyanobacteria (2, 5), and both have transferred most of their genes to the host nuclear genome and are therefore reliant on nuclear-encoded, organelle-targeted proteins for the preservation of crucial biochemical pathways and many repair-, replication-, and expression-related functions (6). Both also show a wide and perplexing assortment of genomic architectures (7,8), which has spurred various evolutionary explanations, ranging from ancient inheritance from the RNA world to selection for greater "evolvability" (9, 10).At first glance, genomic complexity w...

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“…Plastid genomes of diatoms share a core set of 122 protein‐coding genes, 3rRNAs, 27 tRNAs, and two additional RNA genes, tmRNA and ffs (Ruck et al. , Yu et al. ).…”

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confidence: 99%

“…They also vary greatly in size, due to the expansions/contractions of intergenic regions by “anonymous” DNA with unique sequences that are lineage or species specific (Ruck et al. ).…”

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The complete chloroplast and mitochondrial genomes of the diatomNitzschia palea(Bacillariophyceae) demonstrate high sequence similarity to the endosymbiont organelles of the dinotomDurinskia baltica

Crowell

Nienow

Cahoon

2019

Journal of Phycology

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Nitzschia palea is a common freshwater diatom used as a bioindicator because of its tolerance of polluted waterways. There is also evidence it may be the tertiary endosymbiont within the “dinotom” dinoflagellate Durinskia baltica. A putative strain of N. palea was collected from a pond on the University of Virginia's College at Wise campus and cultured. For initial identification, three markers were sequenced—nuclear 18S rDNA, the chloroplast 23S rDNA, and rbcL. Morphological characteristics were determined using light and scanning electron microscopy; based on these observations the cells were identified as N. palea and named strain “Wise.” DNA from N. palea was deep sequenced and the chloroplast and mitochondrial genomes assembled. Single gene phylogenies grouped N. palea—Wise within a clearly defined N. palea clade and showed it was most closely related to the strain “SpainA3.” The chloroplast genome of N. palea is 119,447 bp with a quadripartite structure, 135 protein‐coding, 28 tRNA, and 3 rRNA genes. The mitochondrial genome is 37,754 bp with a single repeat region as found in other diatom chondriomes, 37 protein‐coding, 23 tRNA, and 2 rRNA genes. The chloroplast genomes of N. palea and D. baltica have identical gene content, synteny, and a 92.7% pair‐wise sequence similarity with most differences occurring in intergenic regions. The N. palea mitochondrial genome and D. baltica's endosymbiont mitochondrial genome also have identical gene content and order with a sequence similarity of 90.7%. Genome‐based phylogenies demonstrated that D. baltica is more similar to N. palea than any other diatom sequence currently available. These data provide the genome sequences of two organelles for a widespread diatom and show they are very similar to those of Durinskia baltica's endosymbiont.

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Serial Gene Losses and Foreign DNA Underlie Size and Sequence Variation in the Plastid Genomes of Diatoms

Cited by 65 publications

References 67 publications

Conserved Gene Order and Expanded Inverted Repeats Characterize Plastid Genomes of Thalassiosirales

Conserved Gene Order and Expanded Inverted Repeats Characterize Plastid Genomes of Thalassiosirales

Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes

The complete chloroplast and mitochondrial genomes of the diatomNitzschia palea(Bacillariophyceae) demonstrate high sequence similarity to the endosymbiont organelles of the dinotomDurinskia baltica

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