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Title: Proteomic and Mutant Analysis of the CO2 Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena

Abstract

Many autotrophic microorganisms are likely to adapt to scarcity in dissolved inorganic carbon (DIC; CO2+ HCO3-+ CO32-) with CO2 concentrating mechanisms (CCM) that actively transport DIC across the cell membrane to facilitate carbon fixation. Surprisingly, DIC transport has been well studied among cyanobacteria and microalgae only. The deep-sea vent gammaproteobacterial chemolithoautotrophThiomicrospira crunogenahas a low-DIC inducible CCM, though the mechanism for uptake is unclear, as homologs to cyanobacterial transporters are absent. To identify the components of this CCM, proteomes ofT. crunogenacultivated under low- and high-DIC conditions were compared. Fourteen proteins, including those comprising carboxysomes, were at least 4-fold more abundant under low-DIC conditions. One of these proteins was encoded byTcr_0854; strains carrying mutated copies of this gene, as well as the adjacent Tcr_0853, required elevated DIC for growth. Strains carrying mutated copies of Tcr_0853 and Tcr_0854 overexpressed carboxysomes and had diminished ability to accumulate intracellular DIC. Based on reverse transcription (RT)-PCR, Tcr_0853 and Tcr_0854 were cotranscribed and upregulated under low-DIC conditions. The Tcr_0853 -encoded protein was predicted to have 13 transmembrane helices. Given the mutant phenotypes described above, Tcr_0853 and Tcr_0854 may encode a two-subunit DIC transporter that belongs to a previously undescribed transporter family, though it is widespread among autotrophsmore » from multiple phyla.DIC uptake and fixation by autotrophs are the primary input of inorganic carbon into the biosphere. The mechanism for dissolved inorganic carbon uptake has been characterized only for cyanobacteria despite the importance of DIC uptake by autotrophic microorganisms from many phyla among theBacteriaandArchaea. In this work, proteins necessary for dissolved inorganic carbon utilization in the deep-sea vent chemolithoautotrophT. crunogenawere identified, and two of these may be able to form a novel transporter. Homologs of these proteins are present in 14 phyla inBacteriaand also in one phylum ofArchaea, theEuryarchaeota. Many organisms carrying these homologs are autotrophs, suggesting a role in facilitating dissolved inorganic carbon uptake and fixation well beyond the genusThiomicrospira.« less

Authors:
 [1];  [1];  [2];  [1];  [3];  [1];  [1];  [1];  [1];  [1];  [2];  [1];  [1];  [4];  [1]
+ Show Author Affiliations
  1. Univ. of South Florida, Tampa, FL (United States). Dept. of Integrative Biology
  2. Univ. of South Florida, Tampa, FL (United States). Dept. of Cell Biology, Microbiology, and Molecular Biology
  3. Richard Stockton College of New Jersey, Pomona, NJ (United States). Biology Program
  4. Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology ; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Computer Science and Mathematics Division
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
Contributing Org.:
USF MCB4404L
OSTI Identifier:
1407731
Grant/Contract Number:  
AC05-00OR22725; NSF-MCB-0643713; NSF-IOS-1257532
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Bacteriology
Additional Journal Information:
Journal Volume: 199; Journal Issue: 7; Journal ID: ISSN 0021-9193
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; autotroph; bicarbonate transporter; carbon concentrating mechanism; carbon fixation; chemolithoautotroph; hydrothermal vent

Citation Formats

Mangiapia, Mary, Brown, Terry-René W., Chaput, Dale, Haller, Edward, Harmer, Tara L., Hashemy, Zahra, Keeley, Ryan, Leonard, Juliana, Mancera, Paola, Nicholson, David, Stevens, Stanley, Wanjugi, Pauline, Zabinski, Tania, Pan, Chongle, and Scott, Kathleen M. Proteomic and Mutant Analysis of the CO2 Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena. United States: N. p., 2017. Web. doi:10.1128/JB.00871-16.
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Mangiapia, Mary, Brown, Terry-René W., Chaput, Dale, Haller, Edward, Harmer, Tara L., Hashemy, Zahra, Keeley, Ryan, Leonard, Juliana, Mancera, Paola, Nicholson, David, Stevens, Stanley, Wanjugi, Pauline, Zabinski, Tania, Pan, Chongle, & Scott, Kathleen M. Proteomic and Mutant Analysis of the CO2 Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena. United States. https://doi.org/10.1128/JB.00871-16
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Mangiapia, Mary, Brown, Terry-René W., Chaput, Dale, Haller, Edward, Harmer, Tara L., Hashemy, Zahra, Keeley, Ryan, Leonard, Juliana, Mancera, Paola, Nicholson, David, Stevens, Stanley, Wanjugi, Pauline, Zabinski, Tania, Pan, Chongle, and Scott, Kathleen M. Mon . "Proteomic and Mutant Analysis of the CO2 Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena". United States. https://doi.org/10.1128/JB.00871-16. https://www.osti.gov/servlets/purl/1407731.
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@article{osti_1407731,
title = {Proteomic and Mutant Analysis of the CO2 Concentrating Mechanism of Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena},
author = {Mangiapia, Mary and Brown, Terry-René W. and Chaput, Dale and Haller, Edward and Harmer, Tara L. and Hashemy, Zahra and Keeley, Ryan and Leonard, Juliana and Mancera, Paola and Nicholson, David and Stevens, Stanley and Wanjugi, Pauline and Zabinski, Tania and Pan, Chongle and Scott, Kathleen M.},
abstractNote = {Many autotrophic microorganisms are likely to adapt to scarcity in dissolved inorganic carbon (DIC; CO2+ HCO3-+ CO32-) with CO2 concentrating mechanisms (CCM) that actively transport DIC across the cell membrane to facilitate carbon fixation. Surprisingly, DIC transport has been well studied among cyanobacteria and microalgae only. The deep-sea vent gammaproteobacterial chemolithoautotrophThiomicrospira crunogenahas a low-DIC inducible CCM, though the mechanism for uptake is unclear, as homologs to cyanobacterial transporters are absent. To identify the components of this CCM, proteomes ofT. crunogenacultivated under low- and high-DIC conditions were compared. Fourteen proteins, including those comprising carboxysomes, were at least 4-fold more abundant under low-DIC conditions. One of these proteins was encoded byTcr_0854; strains carrying mutated copies of this gene, as well as the adjacent Tcr_0853, required elevated DIC for growth. Strains carrying mutated copies of Tcr_0853 and Tcr_0854 overexpressed carboxysomes and had diminished ability to accumulate intracellular DIC. Based on reverse transcription (RT)-PCR, Tcr_0853 and Tcr_0854 were cotranscribed and upregulated under low-DIC conditions. The Tcr_0853 -encoded protein was predicted to have 13 transmembrane helices. Given the mutant phenotypes described above, Tcr_0853 and Tcr_0854 may encode a two-subunit DIC transporter that belongs to a previously undescribed transporter family, though it is widespread among autotrophs from multiple phyla.DIC uptake and fixation by autotrophs are the primary input of inorganic carbon into the biosphere. The mechanism for dissolved inorganic carbon uptake has been characterized only for cyanobacteria despite the importance of DIC uptake by autotrophic microorganisms from many phyla among theBacteriaandArchaea. In this work, proteins necessary for dissolved inorganic carbon utilization in the deep-sea vent chemolithoautotrophT. crunogenawere identified, and two of these may be able to form a novel transporter. Homologs of these proteins are present in 14 phyla inBacteriaand also in one phylum ofArchaea, theEuryarchaeota. Many organisms carrying these homologs are autotrophs, suggesting a role in facilitating dissolved inorganic carbon uptake and fixation well beyond the genusThiomicrospira.},
doi = {10.1128/JB.00871-16},
journal = {Journal of Bacteriology},
number = 7,
volume = 199,
place = {United States},
year = {Mon Jan 23 00:00:00 EST 2017},
month = {Mon Jan 23 00:00:00 EST 2017}
}
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https://doi.org/10.1128/JB.00871-16
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Works referenced in this record:

Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus
journal, June 2011

Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: Genes involved and their phylogenetic relationship with homologous genes in other organisms
journal, September 2001

  • Shibata, M.; Ohkawa, H.; Kaneko, T.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 20
  • DOI: 10.1073/pnas.191258298

Phylogenetic Affinity of a Wide, Vacuolate, Nitrate-AccumulatingBeggiatoa sp. from Monterey Canyon, California, withThioploca spp
journal, January 1999

The Carbon-Concentrating Mechanism of the Hydrothermal Vent Chemolithoautotroph Thiomicrospira crunogena
journal, August 2005

Characterization of Anaerobic Catabolism of p -Coumarate in Rhodopseudomonas palustris by Integrating Transcriptomics and Quantitative Proteomics
journal, December 2007

  • Pan, Chongle; Oda, Yasuhiro; Lankford, Patricia K.
  • Molecular & Cellular Proteomics, Vol. 7, Issue 5
  • DOI: 10.1074/mcp.M700147-MCP200

New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010

  • Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
  • Systematic Biology, Vol. 59, Issue 3
  • DOI: 10.1093/sysbio/syq010

An Improved General Amino Acid Replacement Matrix
journal, April 2008

Short-term temperature variability in the Rose Garden hydrothermal vent field: an unstable deep-sea environment
journal, October 1988

  • Johnson, Kenneth S.; Childress, James J.; Beehler, Carl L.
  • Deep Sea Research Part A. Oceanographic Research Papers, Vol. 35, Issue 10-11
  • DOI: 10.1016/0198-0149(88)90045-3

Characterization of two different 2-oxoglutarate:ferredoxin oxidoreductases from Hydrogenobacter thermophilus TK-6
journal, December 2003

  • Yamamoto, Masahiro; Arai, Hiroyuki; Ishii, Masaharu
  • Biochemical and Biophysical Research Communications, Vol. 312, Issue 4
  • DOI: 10.1016/j.bbrc.2003.11.078

Hydrogenase Gene Distribution and H2 Consumption Ability within the Thiomicrospira Lineage
journal, February 2016

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

Bacterial Microcompartments
journal, October 2010

Hem-1 Complexes Are Essential for Rac Activation, Actin Polymerization, and Myosin Regulation during Neutrophil Chemotaxis
journal, January 2006

Transcriptional Response of the Sulfur Chemolithoautotroph Thiomicrospira crunogena to Dissolved Inorganic Carbon Limitation
journal, February 2012

  • Dobrinski, K. P.; Enkemann, S. A.; Yoder, S. J.
  • Journal of Bacteriology, Vol. 194, Issue 8
  • DOI: 10.1128/JB.06504-11

Inorganic carbon transporters of the cyanobacterial CO2 concentrating mechanism
journal, February 2011

The Genera Thiobacillus and Thiomicrospira
book, January 1981

An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database
journal, November 1994

  • Eng, Jimmy K.; McCormack, Ashley L.; Yates, John R.
  • Journal of the American Society for Mass Spectrometry, Vol. 5, Issue 11
  • DOI: 10.1016/1044-0305(94)80016-2

Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments
journal, August 2007

Increased species diversity and extended habitat range of sulfur-oxidizing Thiomicrospira spp.
journal, January 1997

Distribution and Diversity of Sulfur-OxidizingThiomicrospira spp. at a Shallow-Water Hydrothermal Vent in the Aegean Sea (Milos, Greece)
journal, September 1999

Assembly, function and evolution of cyanobacterial carboxysomes
journal, June 2016

Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT
journal, August 2002

  • McDonald, W. Hayes; Ohi, Ryoma; Miyamoto, David T.
  • International Journal of Mass Spectrometry, Vol. 219, Issue 1
  • DOI: 10.1016/S1387-3806(02)00563-8

IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013

  • Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt963

Metagenomic Comparison of Two Thiomicrospira Lineages Inhabiting Contrasting Deep-Sea Hydrothermal Environments
journal, October 2010

ProRata:  A Quantitative Proteomics Program for Accurate Protein Abundance Ratio Estimation with Confidence Interval Evaluation
journal, October 2006

  • Pan, Chongle; Kora, Guruprasad; McDonald, W. Hayes
  • Analytical Chemistry, Vol. 78, Issue 20
  • DOI: 10.1021/ac060654b

Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001

In-gel digestion for mass spectrometric characterization of proteins and proteomes
journal, December 2006

Robust Estimation of Peptide Abundance Ratios and Rigorous Scoring of Their Variability and Bias in Quantitative Shotgun Proteomics
journal, October 2006

  • Pan, Chongle; Kora, Guruprasad; Tabb, David L.
  • Analytical Chemistry, Vol. 78, Issue 20
  • DOI: 10.1021/ac0606554

Bioinformatic analysis of the distribution of inorganic carbon transporters and prospective targets for bioengineering to increase Ci uptake by cyanobacteria
journal, November 2014

  • Gaudana, Sandeep B.; Zarzycki, Jan; Moparthi, Vamsi K.
  • Photosynthesis Research, Vol. 126, Issue 1
  • DOI: 10.1007/s11120-014-0059-8

Purification and Functional Reconstitution of a Seven-Subunit Mrp-Type Na+/H+ Antiporter
journal, October 2013

  • Morino, M.; Suzuki, T.; Ito, M.
  • Journal of Bacteriology, Vol. 196, Issue 1
  • DOI: 10.1128/JB.01029-13

Conditionally Replicative and Conjugative Plasmids CarryinglacZα for Cloning, Mutagenesis, and Allele Replacement in Bacteria
journal, January 1996

  • Metcalf, William W.; Jiang, Weihong; Daniels, Larry L.
  • Plasmid, Vol. 35, Issue 1
  • DOI: 10.1006/plas.1996.0001

Chemical and biological interactions in the Rose Garden hydrothermal vent field, Galapagos spreading center
journal, October 1988

  • Johnson, Kenneth S.; Childress, James J.; Hessler, Robert R.
  • Deep Sea Research Part A. Oceanographic Research Papers, Vol. 35, Issue 10-11
  • DOI: 10.1016/0198-0149(88)90046-5

DTASelect and Contrast:  Tools for Assembling and Comparing Protein Identifications from Shotgun Proteomics
journal, February 2002

  • Tabb, David L.; McDonald, W. Hayes; Yates, John R.
  • Journal of Proteome Research, Vol. 1, Issue 1, p. 21-26
  • DOI: 10.1021/pr015504q

Dissolved inorganic carbon uptake in Thiomicrospira crunogena XCL-2 is Δp- and ATP-sensitive and enhances RubisCO-mediated carbon fixation
journal, November 2015

  • Menning, Kristy J.; Menon, Balaraj B.; Fox, Gordon
  • Archives of Microbiology, Vol. 198, Issue 2
  • DOI: 10.1007/s00203-015-1172-6

Enzymes of a novel autotrophic CO2 fixation pathway in the phototrophic bacterium Chloroflexus aurantiacus, the 3-hydroxypropionate cycle
journal, August 1993

Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms
journal, May 2008

  • Tabita, F. Robert; Hanson, Thomas E.; Satagopan, Sriram
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1504
  • DOI: 10.1098/rstb.2008.0023

An improved arbitrary primed PCR method for rapid characterization of transposon insertion sites
journal, October 2005

Characterization and expression of genes from the RubisCO gene cluster of the chemoautotrophic symbiont of Solemya velum: cbbLSQO
journal, July 2004

  • Schwedock, Julie; Harmer, Tara L.; Scott, Kathleen M.
  • Archives of Microbiology, Vol. 182, Issue 1
  • DOI: 10.1007/s00203-004-0689-x

MUSCLE: multiple sequence alignment with high accuracy and high throughput
journal, March 2004

  • Edgar, R. C.
  • Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797
  • DOI: 10.1093/nar/gkh340

Thiomicrospira crunogena sp. nov., a Colorless, Sulfur-Oxidizing Bacterium from a Deep-Sea Hydrothermal Vent
journal, October 1985

  • Jannasch, H. W.; Wirsen, C. O.; Nelson, D. C.
  • International Journal of Systematic Bacteriology, Vol. 35, Issue 4
  • DOI: 10.1099/00207713-35-4-422

Statistical significance for genomewide studies
journal, July 2003

  • Storey, J. D.; Tibshirani, R.
  • Proceedings of the National Academy of Sciences, Vol. 100, Issue 16, p. 9440-9445
  • DOI: 10.1073/pnas.1530509100

CO 2 Fixation Kinetics of Halothiobacillus neapolitanus Mutant Carboxysomes Lacking Carbonic Anhydrase Suggest the Shell Acts as a Diffusional Barrier for CO 2
journal, February 2008

  • Dou, Zhicheng; Heinhorst, Sabine; Williams, Eric B.
  • Journal of Biological Chemistry, Vol. 283, Issue 16
  • DOI: 10.1074/jbc.M709285200

Ecological Aspects of the Distribution of Different Autotrophic CO 2 Fixation Pathways
journal, January 2011

Long-Term Response toward Inorganic Carbon Limitation in Wild Type and Glycolate Turnover Mutants of the Cyanobacterium Synechocystis sp. Strain PCC 6803
journal, June 2007

  • Eisenhut, Marion; von Wobeser, Eneas Aguirre; Jonas, Ludwig
  • Plant Physiology, Vol. 144, Issue 4
  • DOI: 10.1104/pp.107.103341

The ins and outs of CO 2
journal, October 2015

  • Raven, John A.; Beardall, John
  • Journal of Experimental Botany, Vol. 67, Issue 1
  • DOI: 10.1093/jxb/erv451

Inorganic carbon acquisition by the hydrothermal vent tubeworm Riftia pachyptila depends upon high external PCO2 and upon proton-equivalent ion transport by the worm
journal, March 1997

  • Goffredi, S.; Childress, J.; Desaulniers, N.
  • Journal of Experimental Biology, Vol. 200, Issue 5
  • DOI: 10.1242/jeb.200.5.883

Use of Electroporation To Generate a Thiobacillus neapolitanus Carboxysome Mutant.
journal, January 1995

Identification of the dicyclohexylcarbodiimide-binding subunit of NADH-ubiquinone oxidoreductase (Complex I).
journal, November 1988

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