Parallel evolution of transcriptome architecture during genome reorganization

Yoon, Sung Ho; Reiss, David J; Bare, J. Christopher; Tenenbaum, Dan; Pan, Min; Slagel, Joseph; Moritz, Robert L.; Lim, Sujung; Hackett, Murray; Menon, Angeli Lal; Adams, Michael W. W.; Barnebey, Adam; Yannone, Steven M.; Leigh, John A.; Baliga, Nitin S.

doi:10.1101/gr.122218.111

Cited by 52 publications

(63 citation statements)

References 94 publications

(145 reference statements)

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“…To evaluate the effect of polarity on the functional categorization of genes, the EI of genes in the 209 operons previously identified in M. maripaludis S2 were examined (9). If the insertion of the Tn5 transposon interrupts transcript, genes upstream of a possibly essential gene will always appear possibly essential.…”

Section: Resultsmentioning

confidence: 99%

Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis

Sarmiento

Mrázek

Whitman

2013

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

133

157

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A comprehensive whole-genome analysis of gene function by transposon mutagenesis and deep sequencing methodology has been implemented successfully in a representative of the Archaea domain. Libraries of transposon mutants were generated for the hydrogenotrophic, methanogenic archaeon Methanococcus maripaludis S2 using a derivative of the Tn5 transposon. About 89,000 unique insertions were mapped to the genome, which allowed for the classification of 526 genes or about 30% of the genome as possibly essential or strongly advantageous for growth in rich medium. Many of these genes were homologous to eukaryotic genes that encode fundamental processes in replication, transcription, and translation, providing direct evidence for their importance in Archaea. Some genes classified as possibly essential were unique to the archaeal or methanococcal lineages, such as that encoding DNA polymerase PolD. In contrast, the archaeal homolog to the gene encoding DNA polymerase B was not essential for growth, a conclusion confirmed by construction of an independent deletion mutation. Thus PolD, and not PolB, likely plays a fundamental role in DNA replication in methanococci. Similarly, 121 hypothetical ORFs were classified as possibly essential and likely play fundamental roles in methanococcal information processing or metabolism that are not established outside this group of prokaryotes.Tn-seq | polyploidy | methanogenesis

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Section: Resultsmentioning

confidence: 99%

Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis

Sarmiento

Mrázek

Whitman

2013

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

133

157

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“…The MW56 strain contained the SP1 operon between convergently transcribed genes (encoded by loci PF0574 and PF0575; Figs. S2 and S3) within a ∼100-bp region having little to no transcriptional activity, according to a previous tiling array study of P. furiosus (22). The P. furiosus strains used here are summarized in Table S1.…”

Section: Resultsmentioning

confidence: 99%

Exploiting microbial hyperthermophilicity to produce an industrial chemical, using hydrogen and carbon dioxide

Keller

Schut

Lipscomb

et al. 2013

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

116

103

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Microorganisms can be engineered to produce useful products, including chemicals and fuels from sugars derived from renewable feedstocks, such as plant biomass. An alternative method is to use low potential reducing power from nonbiomass sources, such as hydrogen gas or electricity, to reduce carbon dioxide directly into products. This approach circumvents the overall low efficiency of photosynthesis and the production of sugar intermediates. Although significant advances have been made in manipulating microorganisms to produce useful products from organic substrates, engineering them to use carbon dioxide and hydrogen gas has not been reported. Herein, we describe a unique temperature-dependent approach that confers on a microorganism (the archaeon Pyrococcus furiosus, which grows optimally on carbohydrates at 100°C) the capacity to use carbon dioxide, a reaction that it does not accomplish naturally. This was achieved by the heterologous expression of five genes of the carbon fixation cycle of the archaeon Metallosphaera sedula, which grows autotrophically at 73°C. The engineered P. furiosus strain is able to use hydrogen gas and incorporate carbon dioxide into 3-hydroxypropionic acid, one of the top 12 industrial chemical building blocks. The reaction can be accomplished by cell-free extracts and by whole cells of the recombinant P. furiosus strain. Moreover, it is carried out some 30°C below the optimal growth temperature of the organism in conditions that support only minimal growth but maintain sufficient metabolic activity to sustain the production of 3-hydroxypropionate. The approach described here can be expanded to produce important organic chemicals, all through biological activation of carbon dioxide.

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“…Extensive studies of the transcriptome (Hendrickson et al 2007 and proteome (Xia et al , 2009 showed that genes of the methanogenic pathway are significantly regulated by H 2 . Our recent study on the transcriptome map of M. maripaludis generated a comprehensive list of protein-coding and noncoding RNAs for systems modeling of this organism (Yoon et al 2011).…”

mentioning

confidence: 99%

“…First, we generated a comprehensive list of coding and noncoding RNAs through comparative analysis of the complete transcriptome and a comprehensive PeptideAtlas (Deutsch 2010) for M. maripaludisi.e., genome-wide alignments of a collection of peptides that were experimentally detected across a diverse set of tandem mass spectrometry experiments (Yoon et al 2011;Supplemental Methods). Next, we generated a compendium of over 50 transcriptome profiles from steady-state conditions and during dynamic cellular response to a spectrum of environmental perturbations.…”

mentioning

confidence: 99%

“…Next, we generated a compendium of over 50 transcriptome profiles from steady-state conditions and during dynamic cellular response to a spectrum of environmental perturbations. Along with eight transcriptome data sets from our previous study (Yoon et al 2011), a total of 58 transcriptome profiles of wild-type M. maripaludis MM901 were analyzed using the cMonkey biclustering algorithm ) and the Inferelator algorithm , in order to infer the set of environmental factors (EFs) and transcriptional factors (TFs, sequence-specific DNA-binding proteins that mediate regulation of mRNA transcription) that accurately modeled the dynamic transcriptional changes of genes within each bicluster. The EGRIN model was validated using 56 transcriptome data sets that were not used for the model construction: 52 new transcriptome data sets from several genetic backgrounds that modulated methanogenesis in well-understood schemes and four data sets from our previous work (Costa et al 2013b).…”

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confidence: 99%

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A systems level predictive model for global gene regulation of methanogenesis in a hydrogenotrophic methanogen

et al. 2013

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Methanogens catalyze the critical methane-producing step (called methanogenesis) in the anaerobic decomposition of organic matter. Here, we present the first predictive model of global gene regulation of methanogenesis in a hydrogenotrophic methanogen, Methanococcus maripaludis. We generated a comprehensive list of genes (protein-coding and noncoding) for M. maripaludis through integrated analysis of the transcriptome structure and a newly constructed Peptide Atlas. The environment and gene-regulatory influence network (EGRIN) model of the strain was constructed from a compendium of transcriptome data that was collected over 58 different steady-state and time-course experiments that were performed in chemostats or batch cultures under a spectrum of environmental perturbations that modulated methanogenesis. Analyses of the EGRIN model have revealed novel components of methanogenesis that included at least three additional protein-coding genes of previously unknown function as well as one noncoding RNA. We discovered that at least five regulatory mechanisms act in a combinatorial scheme to intercoordinate key steps of methanogenesis with different processes such as motility, ATP biosynthesis, and carbon assimilation. Through a combination of genetic and environmental perturbation experiments we have validated the EGRIN-predicted role of two novel transcription factors in the regulation of phosphate-dependent repression of formate dehydrogenase-a key enzyme in the methanogenesis pathway. The EGRIN model demonstrates regulatory affiliations within methanogenesis as well as between methanogenesis and other cellular functions.

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Parallel evolution of transcriptome architecture during genome reorganization

Cited by 52 publications

References 94 publications

Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis

Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis

Exploiting microbial hyperthermophilicity to produce an industrial chemical, using hydrogen and carbon dioxide

A systems level predictive model for global gene regulation of methanogenesis in a hydrogenotrophic methanogen

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