Origin of an Alternative Genetic Code in the Extremely Small and GC–Rich Genome of a Bacterial Symbiont

McCutcheon, John P.; McDonald, Bradon R.; Moran, Nancy A.

doi:10.1371/journal.pgen.1000565

Cited by 260 publications

(258 citation statements)

References 53 publications

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“…The same recoding was found and biochemically validated in candidate phylum SR1 very recently 41 , suggesting that this codon reassignment may be phylogenetically widespread in uncharacterized lineages. This expands the known alternative coding for UGA, which has previously been reported for selenocysteine 42 and tryptophan 43,44 . The very low guanine-cytosine content of the Gracilibacteria singlecell genomes (,24%) may have driven the recoding of UGA to a lower guanine-cytosine glycine codon alternative (UGA versus GGN) particularly as glycine is the third most commonly used amino acid (.7% average abundance per genome; Supplementary Fig.…”

Section: Functional Diversity and Novel Findingssupporting

confidence: 77%

Insights into the phylogeny and coding potential of microbial dark matter

Rinke

Schwientek

Sczyrba

et al. 2013

Nature

2,227

2,070

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Genome sequencing enhances our understanding of the biological world by providing blueprints for the evolutionary and functional diversity that shapes the biosphere. However, microbial genomes that are currently available are of limited phylogenetic breadth, owing to our historical inability to cultivate most microorganisms in the laboratory. We apply single-cell genomics to target and sequence 201 uncultivated archaeal and bacterial cells from nine diverse habitats belonging to 29 major mostly uncharted branches of the tree of life, so-called 'microbial dark matter'. With this additional genomic information, we are able to resolve many intra-and inter-phylum-level relationships and to propose two new superphyla. We uncover unexpected metabolic features that extend our understanding of biology and challenge established boundaries between the three domains of life. These include a novel amino acid use for the opal stop codon, an archaeal-type purine synthesis in Bacteria and complete sigma factors in Archaea similar to those in Bacteria. The single-cell genomes also served to phylogenetically anchor up to 20% of metagenomic reads in some habitats, facilitating organism-level interpretation of ecosystem function. This study greatly expands the genomic representation of the tree of life and provides a systematic step towards a better understanding of biological evolution on our planet.Microorganisms are the most diverse and abundant cellular life forms on Earth, occupying every possible metabolic niche. The large majority of these organisms have not been obtained in pure culture and we have only recently become aware of their presence mainly through cultivationindependent molecular surveys based on conserved marker genes (chiefly small subunit ribosomal RNA; SSU rRNA) or through shotgun sequencing (metagenomics) 1,2 . As an increasing number of environments are deeply sequenced using next-generation technologies, diversity estimates for Bacteria and Archaea continue to rise, with the number of microbial 'species' predicted to reach well into the millions 3 . According to SSU rRNA-based phylogeny, these fall into at least 60 major lines of descent (phyla or divisions) within the bacterial and archaeal domains 4

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Section: Functional Diversity and Novel Findingssupporting

confidence: 77%

Insights into the phylogeny and coding potential of microbial dark matter

Rinke

Schwientek

Sczyrba

et al. 2013

Nature

2,227

2,070

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“…For example, changes to the genetic code are expected to occur more frequently in genomes with a small amount of protein-coding sequence (99). Likewise, a smaller gene complement could also allow for larger fluctuations in mutation rates because selection against a mutator allele would be proportional to its effect on the rate of functionally deleterious mutations per genome (not per nucleotide).…”

Section: Understanding Mitochondrial and Plastid Genome Evolutionmentioning

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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“…However, genomes of several bacterial endosymbionts in various insects are reduced to organellar sizes (e.g. Hodgkinia cicadicola, 0.144 Mbp; Carsonella ruddii, 0.160 Mbp; Sulcia muelleri, 0.246 Mbp) [106][107][108] and in some cases genome reduction involves the loss of genes involved in DNA replication, transcription, and translation (i.e. functions that occur in the endosymbiont but that are not readily compensated for at the metabolite level) [109].…”

Section: Transitions From Endosymbionts To Organellesmentioning

confidence: 99%

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

Nowack

2014

Acta Soc Bot Pol

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The evolution of plastidsPrimary plastids, the photosynthetic organelles of Plantae (i.e. green algae/land plants, red algae, and glaucophytes) evolved more than 1 billion years ago (gya) through the endosymbiotic uptake of a cyanobacterium by a heterotrophic protist host [1][2][3]. Photosynthetic carbon fixation from the newly acquired plastid relieved the host from its dependency on the continuous uptake of organic carbon molecules from the environment. In addition to photosynthetic carbon fixation, plastids provide other beneficial metabolic functions to the plant/algal cell such as the assimilation of ammonia and sulfate into amino acids [4], assembly of iron-sulfur clusters [5], de novo biosynthesis of fatty acids [6], isopentenyl diphosphate (IPP) [7], and aromatic amino acids [8]; and they contribute to pathways that are distributed over several compartments, such as photorespiration and biosynthesis of pyrimidines and folates [9][10][11].Evolution of plastids was accompanied by a strong reduction of the size of the cyanobacterial genome and the transfer of thousands of cyanobacterial genes into the host nuclear genome, a process termed endosymbiotic gene transfer (EGT) [12,13]. This resulted in proteins localized to the cyanobacterium, now a full-fledged plastid, being synthesized in the cytoplasm and then imported into the plastid through a sophisticated import machinery (the TIC/ TOC complex; short for: translocon of the inner and outer chloroplast membranes) targeted by N-terminal transit peptides [14]. A multitude of solute transporters underlie the intricate metabolic crosstalk between plastid and the surrounding cell by controlling fluxes of metabolites and ions through the double membrane system that delimits the plastid [15][16][17]. Signaling pathways from and to the plastid communicate environmental cues and the metabolic and developmental status of different compartments within the plant/algal cell [18,19]. An interplay of eukaryote-and cyanobacterium-derived proteins coordinate plastid division with the host cell cycle [20].Following the establishment of primary plastids in Plantae, photosynthetic ability spread to other eukaryotic lineages through secondary endosymbioses [21,22]. In secondary endosymbioses a red or green alga served as an endosymbiont, leading to the establishment of secondary plastids in heterokontophytes (stramenopiles), cryptophytes, haptophytes, dinoflagellates, apicomplexa, chlorarachniophytes, and euglenophytes. In most cases the only remnant of the eukaryotic symbiont is one or two extra membranes that surround the secondary plastid. The nuclear genome of the * Email: e.nowack@uni-duesseldorf.deHandling Editor: Andrzej Bodył INVITED REVIEW Acta Soc Bot Pol 83(4): 387-397 DOI: 10.5586/asbp.2014.049 Received: 2014-11-16 Accepted: 2014-12-19 Published electronically: 2014 Paulinella chromatophora -rethinking the transition from endosymbiont to organelle Eva C.M. Nowack* Department of Biology, Heinrich-Heine-Universität Düsseldorf, Universitätsstrasse 1, 40225 Düsseldorf...

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Origin of an Alternative Genetic Code in the Extremely Small and GC–Rich Genome of a Bacterial Symbiont

Cited by 260 publications

References 53 publications

Insights into the phylogeny and coding potential of microbial dark matter

Insights into the phylogeny and coding potential of microbial dark matter

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

Paulinella chromatophora – rethinking the transition from endosymbiont to organelle

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