The Growth and Survival of Mycobacterium smegmatis Is Enhanced by Co-Metabolism of Atmospheric H2
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{"title"=>"The growth and survival of Mycobacterium smegmatis is enhanced by co-metabolism of atmospheric H2", "type"=>"journal", "authors"=>[{"first_name"=>"Chris", "last_name"=>"Greening", "scopus_author_id"=>"55974617000"}, {"first_name"=>"Silas G.", "last_name"=>"Villas-Bôas", "scopus_author_id"=>"8509310900"}, {"first_name"=>"Jennifer R.", "last_name"=>"Robson", "scopus_author_id"=>"7103097384"}, {"first_name"=>"Michael", "last_name"=>"Berney", "scopus_author_id"=>"13103442800"}, {"first_name"=>"Gregory M.", "last_name"=>"Cook", "scopus_author_id"=>"7401953860"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84904792498", "pmid"=>"25058581", "doi"=>"10.1371/journal.pone.0103034", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"373618145", "sgr"=>"84904792498"}, "id"=>"ed559d17-dbff-3843-9e48-e0815cfe7474", "abstract"=>"The soil bacterium Mycobacterium smegmatis is able to scavenge the trace concentrations of H2 present in the atmosphere, but the physiological function and importance of this activity is not understood. We have shown that atmospheric H2 oxidation in this organism depends on two phylogenetically and kinetically distinct high-affinity hydrogenases, Hyd1 (MSMEG_2262-2263) and Hyd2 (MSMEG_2720-2719). In this study, we explored the effect of deleting Hyd2 on cellular physiology by comparing the viability, energetics, transcriptomes, and metabolomes of wild-type vs. Δhyd2 cells. The long-term survival of the Δhyd2 mutant was significantly reduced compared to the wild-type. The mutant additionally grew less efficiently in a range of conditions, most notably during metabolism of short-chain fatty acids; there was a twofold reduction in growth rate and growth yield of the Δhyd2 strain when acetate served as the sole carbon source. Hyd1 compensated for loss of Hyd2 when cells were grown in a high H2 atmosphere. Analysis of cellular parameters showed that Hyd2 was not necessary to generate the membrane potential, maintain intracellular pH homeostasis, or sustain redox balance. However, microarray analysis indicated that Δhyd2 cells were starved for reductant and compensated by rewiring central metabolism; transcripts encoding proteins responsible for oxidative decarboxylation pathways, the urea cycle, and ABC transporter-mediated import were significantly more abundant in the Δhyd2 mutant. Metabolome profiling consistently revealed an increase in intracellular amino acids in the Δhyd2 mutant. We propose that atmospheric H2 oxidation has two major roles in mycobacterial cells: to generate reductant during mixotrophic growth and to sustain the respiratory chain during dormancy.", "link"=>"http://www.mendeley.com/research/growth-survival-mycobacterium-smegmatis-enhanced-cometabolism-atmospheric-h2", "reader_count"=>23, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>2, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>11, "Chemistry"=>2, "Immunology and Microbiology"=>1, "Earth and Planetary Sciences"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"United Kingdom"=>1, "Russia"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1608323", "https://ndownloader.figshare.com/files/1608331", "https://ndownloader.figshare.com/files/1608330", "https://ndownloader.figshare.com/files/1608329", "https://ndownloader.figshare.com/files/1608328", "https://ndownloader.figshare.com/files/1608327", "https://ndownloader.figshare.com/files/1608326", "https://ndownloader.figshare.com/files/1608325", "https://ndownloader.figshare.com/files/1608324", "https://ndownloader.figshare.com/files/1608332"], "description"=>"<div><p>The soil bacterium <i>Mycobacterium smegmatis</i> is able to scavenge the trace concentrations of H<sub>2</sub> present in the atmosphere, but the physiological function and importance of this activity is not understood. We have shown that atmospheric H<sub>2</sub> oxidation in this organism depends on two phylogenetically and kinetically distinct high-affinity hydrogenases, Hyd1 (MSMEG_2262-2263) and Hyd2 (MSMEG_2720-2719). In this study, we explored the effect of deleting Hyd2 on cellular physiology by comparing the viability, energetics, transcriptomes, and metabolomes of wild-type vs. Δ<i>hyd</i>2 cells. The long-term survival of the Δ<i>hyd2</i> mutant was significantly reduced compared to the wild-type. The mutant additionally grew less efficiently in a range of conditions, most notably during metabolism of short-chain fatty acids; there was a twofold reduction in growth rate and growth yield of the Δ<i>hyd</i>2 strain when acetate served as the sole carbon source. Hyd1 compensated for loss of Hyd2 when cells were grown in a high H<sub>2</sub> atmosphere. Analysis of cellular parameters showed that Hyd2 was not necessary to generate the membrane potential, maintain intracellular pH homeostasis, or sustain redox balance. However, microarray analysis indicated that Δ<i>hyd</i>2 cells were starved for reductant and compensated by rewiring central metabolism; transcripts encoding proteins responsible for oxidative decarboxylation pathways, the urea cycle, and ABC transporter-mediated import were significantly more abundant in the Δ<i>hyd2</i> mutant. Metabolome profiling consistently revealed an increase in intracellular amino acids in the Δ<i>hyd</i>2 mutant. We propose that atmospheric H<sub>2</sub> oxidation has two major roles in mycobacterial cells: to generate reductant during mixotrophic growth and to sustain the respiratory chain during dormancy.</p></div>", "links"=>[], "tags"=>["microbiology", "bacteriology", "Bacterial physiology", "Bacterial spores", "Bacterial biochemistry", "Gram positive bacteria", "Microbial physiology", "Microbial metabolism", "microbial ecology", "enhanced", "co-metabolism", "atmospheric"], "article_id"=>1117068, "categories"=>["Biological Sciences"], "users"=>["Chris Greening", "Silas G. Villas-Boas", "Jennifer R. Robson", "Michael Berney", "Gregory M. Cook"], "doi"=>[nil, nil, nil, nil, nil, nil, nil, nil, nil, nil], "stats"=>{"downloads"=>14, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Growth_and_Survival_of_i_Mycobacterium_smegmatis_i_Is_Enhanced_by_Co_Metabolism_of_Atmospheric_H_sub_2_sub_/1117068", "title"=>"The Growth and Survival of <i>Mycobacterium smegmatis</i> Is Enhanced by Co-Metabolism of Atmospheric H<sub>2</sub>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-07-24 03:40:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1608320"], "description"=>"<p>Error margins represent standard deviations from three biological replicates.</p>", "links"=>[], "tags"=>["microbiology", "bacteriology", "Bacterial physiology", "Bacterial spores", "Bacterial biochemistry", "Gram positive bacteria", "Microbial physiology", "Microbial metabolism", "microbial ecology", "wild-type", "cells", "hours", "induction", "stationary"], "article_id"=>1117065, "categories"=>["Biological Sciences"], "users"=>["Chris Greening", "Silas G. Villas-Boas", "Jennifer R. Robson", "Michael Berney", "Gregory M. Cook"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103034.t001", "stats"=>{"downloads"=>3, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Energetic_parameters_of_wild_type_and_i_hyd_i_2_cells_two_hours_following_the_induction_of_stationary_phase_/1117065", "title"=>"Energetic parameters of wild-type and Δ<i>hyd</i>2 cells two hours following the induction of stationary phase.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-07-24 03:40:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1608318"], "description"=>"<p>Metabolites were detected by gas chromatography-mass spectrometry (GC/MS). The values show the relative abundance of each metabolite detected in the samples (arbitrary units) on a logarithmic scale. Legend: Green = Wild-type, Yellow = Δ<i>hyd</i>2. Means were calculated from three biological replicates and five technical replicates for each strain. <i>p</i> values were determined using a Student’s T-test. * = <i>p</i>&lt;0.05, ** = <i>p</i>&lt;0.01 difference relative to wild-type bars.</p>", "links"=>[], "tags"=>["microbiology", "bacteriology", "Bacterial physiology", "Bacterial spores", "Bacterial biochemistry", "Gram positive bacteria", "Microbial physiology", "Microbial metabolism", "microbial ecology", "intracellular", "metabolites", "wild-type"], "article_id"=>1117063, "categories"=>["Biological Sciences"], "users"=>["Chris Greening", "Silas G. Villas-Boas", "Jennifer R. Robson", "Michael Berney", "Gregory M. Cook"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103034.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Profiles_of_intracellular_metabolites_in_i_hyd_i_2_vs_wild_type_cells_/1117063", "title"=>"Profiles of intracellular metabolites in Δ<i>hyd</i>2 vs. wild-type cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 03:40:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1608319"], "description"=>"<p>Cells lacking Hyd2 compensate for the loss of electrons derived from H<sub>2</sub> by increasing oxidation of organic carbon sources. There is an increased flux though the tricarboxylic acid cycle due to upregulation of enzymes involved in oxidative decarboxylation (e.g. ketoglutarate-ferredoxin oxidoreductase) (highlighted in yellow) and downregulation of those involved in anaplerosis (i.e. isocitrate lyase) (highlighted in blue). We model that loss of CO<sub>2</sub> through oxidative decarboxylation reactions is principally responsible for the decreased biomass of Δ<i>hyd</i>2 cells. Oxidative pathways are depicted with green arrows, whereas reductive pathways are represented with blue arrows. The red text shows the expression ratios of the significantly upregulated or downregulated genes in Δ<i>hyd</i>2 vs. wild-type cells.</p>", "links"=>[], "tags"=>["microbiology", "bacteriology", "Bacterial physiology", "Bacterial spores", "Bacterial biochemistry", "Gram positive bacteria", "Microbial physiology", "Microbial metabolism", "microbial ecology", "carbon", "metabolism"], "article_id"=>1117064, "categories"=>["Biological Sciences"], "users"=>["Chris Greening", "Silas G. Villas-Boas", "Jennifer R. Robson", "Michael Berney", "Gregory M. Cook"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103034.g005", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Altered_balance_of_catabolic_anabolic_carbon_metabolism_in_i_hyd_i_2_cells_/1117064", "title"=>"Altered balance of catabolic/anabolic carbon metabolism in Δ<i>hyd</i>2 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 03:40:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1608317"], "description"=>"<p>Both strains were grown synchronously on HdB minimal medium supplemented with 22&gt;2.0, <i>p</i> value≤0.05. The genes were classified as significantly downregulated if expression ratio &lt;0.5, <i>p</i> value≤0.05. The number of genes affected are listed by functional category. The full list of genes in each category is shown in <b><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0103034#pone.0103034.s007\" target=\"_blank\">Table S4</a></b>, <b><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0103034#pone.0103034.s008\" target=\"_blank\">Table S5</a></b>, and <b><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0103034#pone.0103034.s010\" target=\"_blank\">Dataset S1</a></b>.</p>", "links"=>[], "tags"=>["microbiology", "bacteriology", "Bacterial physiology", "Bacterial spores", "Bacterial biochemistry", "Gram positive bacteria", "Microbial physiology", "Microbial metabolism", "microbial ecology", "wild-type"], "article_id"=>1117062, "categories"=>["Biological Sciences"], "users"=>["Chris Greening", "Silas G. Villas-Boas", "Jennifer R. Robson", "Michael Berney", "Gregory M. Cook"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103034.g003", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Genes_with_significant_changes_in_expression_in_i_hyd_i_2_vs_wild_type_cells_/1117062", "title"=>"Genes with significant changes in expression in Δ<i>hyd</i>2 vs. wild-type cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 03:40:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1608316"], "description"=>"<p>Strains were grown on HdB minimal medium. (A) Growth on 5.5 mM glycerol. (B) Complementation on 5.5 mM glycerol in the presence of 50 µg mL<sup>−1</sup> hygromycin. (C) Growth on 12.5 mM acetate. (D) Partial complementation on 12.5 mM acetate in the presence of 50 µg mL<sup>−1</sup> hygromycin. (E) Growth on 12.5 mM acetate in serum vials injected with 10% pure N<sub>2</sub>. (F) Growth on 12.5 mM acetate in serum vials injected with 10% pure H<sub>2</sub>. Legend: Blue circles = Wild-type (or wild-type with empty pOLYG vector for complementation); Red squares = Δ<i>hyd</i>123; Orange point-up triangles = Δ<i>hyd</i>1; Purple point-down triangles = Δ<i>hyd</i>2 (or Δ<i>hyd</i>2 with empty pOLYG vector for complementation); and Grey diamonds = Δ<i>hyd</i>2 with pOLYG vector expressing MSMEG_2720-2719. Error bars show standard deviations from biological triplicates.</p>", "links"=>[], "tags"=>["microbiology", "bacteriology", "Bacterial physiology", "Bacterial spores", "Bacterial biochemistry", "Gram positive bacteria", "Microbial physiology", "Microbial metabolism", "microbial ecology", "mutant"], "article_id"=>1117061, "categories"=>["Biological Sciences"], "users"=>["Chris Greening", "Silas G. Villas-Boas", "Jennifer R. Robson", "Michael Berney", "Gregory M. Cook"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103034.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Observation_complementation_and_recovery_of_mutant_growth_phenotypes_/1117061", "title"=>"Observation, complementation, and recovery of mutant growth phenotypes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 03:40:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/1608315"], "description"=>"<p>(A) Growth of <i>M. smegmatis</i> mc<sup>2</sup>155 and <i>hyd</i> mutants into carbon-limitation. (B) Survival of <i>M. smegmatis</i> mc<sup>2</sup>155 and <i>hyd</i> mutants during carbon-limitation. The strains were grown in aerated conical flasks on HdB minimal medium supplemented with 22 mM glycerol. Growth is shown in OD<sub>600</sub>. Survival is shown in percentage colony forming units relative to day four. Legend: Blue circles/bars = Wild-type; Red squares/bars = Δ<i>hyd</i>123; Orange point-up triangles/bars = Δ<i>hyd</i>1; and Purple point-down triangles/bars = Δ<i>hyd</i>2. Error bars show standard deviations from biological triplicates. * = <i>p</i>&lt;0.05, ** = <i>p</i>&lt;0.01, *** = <i>p</i>&lt;0.001 difference relative to wild-type bars (Student’s T-test, unpaired, two-tailed).</p>", "links"=>[], "tags"=>["microbiology", "bacteriology", "Bacterial physiology", "Bacterial spores", "Bacterial biochemistry", "Gram positive bacteria", "Microbial physiology", "Microbial metabolism", "microbial ecology", "absences"], "article_id"=>1117060, "categories"=>["Biological Sciences"], "users"=>["Chris Greening", "Silas G. Villas-Boas", "Jennifer R. Robson", "Michael Berney", "Gregory M. Cook"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103034.g001", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_growth_and_survival_of_i_Mycobacterium_smegmatis_i_in_the_presence_and_absences_of_hydrogenases_/1117060", "title"=>"The growth and survival of <i>Mycobacterium smegmatis</i> in the presence and absences of hydrogenases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 03:40:24"}

PMC Usage Stats | Further Information

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Relative Metric

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