Identification of a parasitic symbiosis between respiratory metabolisms in the biogeochemical chlorine cycle

Barnum, Tyler P.; Cheng, Yiwei; Hill, Kaisle A.; Lucas, Lauren N.; Carlson, Hans K.; Coates, John D.

doi:10.1038/s41396-020-0599-1

Identification of a parasitic symbiosis between respiratory metabolisms in the biogeochemical chlorine cycle

Journal Article · Wed Feb 05 00:00:00 EST 2020 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-020-0599-1· OSTI ID:1633283

Barnum, Tyler P. ^[1]; Cheng, Yiwei ^[2]; ^[1]; Lucas, Lauren N. ^[1]; Carlson, Hans K. ^[2]; Coates, John D. ^[1]

Univ. of California, Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

A key step in the chlorine cycle is the reduction of perchlorate (ClO₄^-) and chlorate (ClO₃^-) to chloride by microbial respiratory pathways. Perchlorate-reducing bacteria and chlorate-reducing bacteria differ in that the latter cannot use perchlorate, the most oxidized chlorine compound. However, a recent study identified a bacterium with the chlorate reduction pathway dominating a community provided only perchlorate. Here we confirm a metabolic interaction between perchlorate- and chlorate-reducing bacteria and define its mechanism. Perchlorate-reducing bacteria supported the growth of chlorate-reducing bacteria to up to 90% of total cells in communities and co-cultures. Chlorate-reducing bacteria required the gene for chlorate reductase to grow in co-culture with perchlorate-reducing bacteria, demonstrating that chlorate is responsible for the interaction, not the subsequent intermediates chlorite and oxygen. Modeling of the interaction suggested that cells specialized for chlorate reduction have a competitive advantage for consuming chlorate produced from perchlorate, especially at high concentrations of perchlorate, because perchlorate and chlorate compete for a single enzyme in perchlorate-reducing cells. We conclude that perchlorate-reducing bacteria inadvertently support large populations of chlorate-reducing bacteria in a parasitic relationship through the release of the intermediate chlorate. An implication of these findings is that undetected chlorate-reducing bacteria have likely negatively impacted efforts to bioremediate perchlorate pollution for decades.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Science Foundation (NSF); USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1633283

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 5 Vol. 14; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Chlorite dismutases - a heme enzyme family for use in bioremediation and generation of molecular oxygen Hofbauer, Stefan; Schaffner, Irene; Furtmüller, Paul G. Biotechnology Journal, Vol. 9, Issue 4 https://doi.org/10.1002/biot.201300210	journal	February 2014
Desulfuromonas palmitatis sp. nov., a marine dissimilatory Fe(III) reducer that can oxidize long-chain fatty acids Coates, John D.; Lonergan, Debra J.; Philips, Elizabeth J. P. Archives of Microbiology, Vol. 164, Issue 6 https://doi.org/10.1007/BF02529738	journal	December 1995
Desulfuromonas palmitatis sp. nov., a marine dissimilatory Fe(III) reducer that can oxidize long-chain fatty acids Coates, John D.; Lonergan, Debra J.; Philips, Elizabeth J. P. Archives of Microbiology, Vol. 164, Issue 6 https://doi.org/10.1007/s002030050282	journal	December 1995
Purification and characterization of chlorite dismutase: a novel oxygen-generating enzyme van Ginkel, C. G.; Rikken, G. B.; Kroon, A. G. M. Archives of Microbiology, Vol. 166, Issue 5 https://doi.org/10.1007/s002030050390	journal	November 1996
Description of the novel perchlorate-reducing bacteria Dechlorobacter hydrogenophilus gen. nov., sp. nov. and Propionivibrio militaris, sp. nov. Thrash, J. Cameron; Pollock, Jarrod; Torok, Tamas Applied Microbiology and Biotechnology, Vol. 86, Issue 1 https://doi.org/10.1007/s00253-009-2336-6	journal	November 2009
Characterization of an anaerobic marine microbial community exposed to combined fluxes of perchlorate and salinity Carlström, Charlotte I.; Lucas, Lauren N.; Rohde, Robert A. Applied Microbiology and Biotechnology, Vol. 100, Issue 22 https://doi.org/10.1007/s00253-016-7780-5	journal	September 2016
Transformation of (per)chlorate into chloride by a newly isolated bacterium: reduction and dismutation Rikken, G. B.; Kroon, A. G. M.; van Ginkel, C. G. Applied Microbiology and Biotechnology, Vol. 45, Issue 3 https://doi.org/10.1007/s002530050707	journal	April 1996
Ideonella dechloratans gen.nov., sp.nov., a New Bacterium Capable of Growing Anaerobically with Chlorate as an Electron Acceptor Malmqvist, Åsa; Welander, Thomas; Moore, Edward Systematic and Applied Microbiology, Vol. 17, Issue 1 https://doi.org/10.1016/S0723-2020(11)80032-9	journal	March 1994
Characterisation of chlorate reduction in the haloarchaeon Haloferax mediterranei Martínez-Espinosa, Rosa María; Richardson, David J.; Bonete, María José Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1850, Issue 4 https://doi.org/10.1016/j.bbagen.2014.12.011	journal	April 2015
Why is metabolic labour divided in nitrification? Costa, Engràcia; Pérez, Julio; Kreft, Jan-Ulrich Trends in Microbiology, Vol. 14, Issue 5 https://doi.org/10.1016/j.tim.2006.03.006	journal	May 2006
A New Perspective on Microbes Formerly Known as Nitrite-Oxidizing Bacteria Daims, Holger; Lücker, Sebastian; Wagner, Michael Trends in Microbiology, Vol. 24, Issue 9 https://doi.org/10.1016/j.tim.2016.05.004	journal	September 2016
Genomics and Ecology of Novel N2O-Reducing Microorganisms Hallin, Sara; Philippot, Laurent; Löffler, Frank E. Trends in Microbiology, Vol. 26, Issue 1 https://doi.org/10.1016/j.tim.2017.07.003	journal	January 2018
Kinetics of a hydrogen-oxidizing, perchlorate-reducing bacterium Nerenberg, Robert; Kawagoshi, Yasunori; Rittmann, Bruce E. Water Research, Vol. 40, Issue 17 https://doi.org/10.1016/j.watres.2006.06.035	journal	October 2006
Kinetics of a chlorate-accumulating, perchlorate-reducing bacterium Dudley, Margaret; Salamone, Anna; Nerenberg, Robert Water Research, Vol. 42, Issue 10-11 https://doi.org/10.1016/j.watres.2008.01.009	journal	May 2008
Abiotic Reduction of Chlorate by Fe(II) Minerals: Implications for Occurrence and Transformation of Oxy-Chlorine Species on Earth and Mars Brundrett, Maeghan; Yan, Weile; Velazquez, Maria C. ACS Earth and Space Chemistry, Vol. 3, Issue 5 https://doi.org/10.1021/acsearthspacechem.8b00206	journal	February 2019
A Dimeric Chlorite Dismutase Exhibits O ₂ -Generating Activity and Acts as a Chlorite Antioxidant in Klebsiella pneumoniae MGH 78578 Celis, Arianna I.; Geeraerts, Zachary; Ngmenterebo, David Biochemistry, Vol. 54, Issue 2 https://doi.org/10.1021/bi501184c	journal	December 2014
Perchlorate in Wet Deposition Across North America Rajagopalan, Srinath; Anderson, Todd; Cox, Stephen Environmental Science & Technology, Vol. 43, Issue 3 https://doi.org/10.1021/es801737u	journal	February 2009
Discovery of Natural Perchlorate in the Antarctic Dry Valleys and Its Global Implications Kounaves, Samuel P.; Stroble, Shannon T.; Anderson, Rachel M. Environmental Science & Technology, Vol. 44, Issue 7 https://doi.org/10.1021/es9033606	journal	April 2010
Segregating metabolic processes into different microbial cells accelerates the consumption of inhibitory substrates Lilja, Elin E.; Johnson, David R. The ISME Journal, Vol. 10, Issue 7 https://doi.org/10.1038/ismej.2015.243	journal	January 2016
Exact sequence variants should replace operational taxonomic units in marker-gene data analysis Callahan, Benjamin J.; McMurdie, Paul J.; Holmes, Susan P. The ISME Journal, Vol. 11, Issue 12 https://doi.org/10.1038/ismej.2017.119	journal	July 2017
Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria Martens-Habbena, Willm; Berube, Paul M.; Urakawa, Hidetoshi Nature, Vol. 461, Issue 7266 https://doi.org/10.1038/nature08465	journal	September 2009
Complete nitrification by Nitrospira bacteria Daims, Holger; Lebedeva, Elena V.; Pjevac, Petra Nature, Vol. 528, Issue 7583 https://doi.org/10.1038/nature16461	journal	November 2015
Reconciling the chemistry and biology of reactive oxygen species Winterbourn, Christine C. Nature Chemical Biology, Vol. 4, Issue 5 https://doi.org/10.1038/nchembio.85	journal	April 2008
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system Anantharaman, Karthik; Brown, Christopher T.; Hug, Laura A. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms13219	journal	October 2016
DADA2: High-resolution sample inference from Illumina amplicon data Callahan, Benjamin J.; McMurdie, Paul J.; Rosen, Michael J. Nature Methods, Vol. 13, Issue 7 https://doi.org/10.1038/nmeth.3869	journal	May 2016
Microbial perchlorate reduction: rocket-fuelled metabolism Coates, John D.; Achenbach, Laurie A. Nature Reviews Microbiology, Vol. 2, Issue 7 https://doi.org/10.1038/nrmicro926	journal	July 2004
Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle Anantharaman, Karthik; Hausmann, Bela; Jungbluth, Sean P. The ISME Journal, Vol. 12, Issue 7 https://doi.org/10.1038/s41396-018-0078-0	journal	February 2018
Genome-resolved metagenomics identifies genetic mobility, metabolic interactions, and unexpected diversity in perchlorate-reducing communities Barnum, Tyler P.; Figueroa, Israel A.; Carlström, Charlotte I. The ISME Journal, Vol. 12, Issue 6 https://doi.org/10.1038/s41396-018-0081-5	journal	February 2018
Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander Song, Xiaoming; Nie, Fulei; Chen, Wei Horticulture Research, Vol. 7, Issue 1 https://doi.org/10.1038/s41438-020-0261-0	journal	April 2020
From chlorite dismutase towards HemQ–the role of the proximal H-bonding network in haeme binding Hofbauer, Stefan; Howes, Barry D.; Flego, Nicola Bioscience Reports, Vol. 36, Issue 2 https://doi.org/10.1042/BSR20150330	journal	March 2016
Complete conversion of nitrate into dinitrogen gas in co-cultures of denitrifying bacteria Van de Pas-Schoonen, K. T.; Schalk-Otte, S.; Haaijer, S. Biochemical Society Transactions, Vol. 33, Issue 1 https://doi.org/10.1042/BST0330205	journal	February 2005
Perchlorate Reductase Is Distinguished by Active Site Aromatic Gate Residues Youngblut, Matthew D.; Tsai, Chi-Lin; Clark, Iain C. Journal of Biological Chemistry, Vol. 291, Issue 17 https://doi.org/10.1074/jbc.M116.714618	journal	March 2016
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
Bandage: interactive visualization of de novo genome assemblies: Fig. 1. Wick, Ryan R.; Schultz, Mark B.; Zobel, Justin Bioinformatics, Vol. 31, Issue 20 https://doi.org/10.1093/bioinformatics/btv383	journal	June 2015
Synthetic microbial ecology and the dynamic interplay between microbial genotypes Dolinšek, Jan; Goldschmidt, Felix; Johnson, David R. FEMS Microbiology Reviews, Vol. 40, Issue 6 https://doi.org/10.1093/femsre/fuw024	journal	August 2016
HMMER web server: 2015 update Finn, Robert D.; Clements, Jody; Arndt, William Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv397	journal	May 2015
Efficient de novo assembly of large genomes using compressed data structures Simpson, J. T.; Durbin, R. Genome Research, Vol. 22, Issue 3 https://doi.org/10.1101/gr.126953.111	journal	December 2011
Genetic dissection of chlorate respiration in P seudomonas stutzeri PDA reveals syntrophic (per)chlorate reduction : Symbiotic (per)chlorate respiration Clark, Iain C.; Youngblut, Matt; Jacobsen, Gillian Environmental Microbiology, Vol. 18, Issue 10 https://doi.org/10.1111/1462-2920.13068	journal	December 2015
Perchlorate and chlorate reduction by the Crenarchaeon A eropyrum pernix and two thermophilic Firmicutes: Perchlorate reduction by (hyper)thermophiles Liebensteiner, Martin G.; Pinkse, Martijn W. H.; Nijsse, Bart Environmental Microbiology Reports, Vol. 7, Issue 6 https://doi.org/10.1111/1758-2229.12335	journal	October 2015
Chlorate reduction in S hewanella algae ACDC is a recently acquired metabolism characterized by gene loss, suboptimal regulation and oxidative stress : Chlorate reduction in Clark, Iain C.; Melnyk, Ryan A.; Iavarone, Anthony T. Molecular Microbiology, Vol. 94, Issue 1 https://doi.org/10.1111/mmi.12746	journal	September 2014
Microbial respiration with chlorine oxyanions: diversity and physiological and biochemical properties of chlorate- and perchlorate-reducing microorganisms: Microbial reduction of chlorine oxyanions Liebensteiner, Martin G.; Oosterkamp, Margreet J.; Stams, Alfons J. M. Annals of the New York Academy of Sciences, Vol. 1365, Issue 1 https://doi.org/10.1111/nyas.12806	journal	June 2015
Archaeal (Per)Chlorate Reduction at High Temperature: An Interplay of Biotic and Abiotic Reactions Liebensteiner, Martin G.; Pinkse, Martijn W. H.; Schaap, Peter J. Science, Vol. 340, Issue 6128 https://doi.org/10.1126/science.1233957	journal	April 2013
Magnetospirillum bellicus sp. nov., a Novel Dissimilatory Perchlorate-Reducing Alphaproteobacterium Isolated from a Bioelectrical Reactor Thrash, J. Cameron; Ahmadi, Sarir; Torok, Tamas Applied and Environmental Microbiology, Vol. 76, Issue 14 https://doi.org/10.1128/AEM.00015-10	journal	May 2010
Identification of a Perchlorate Reduction Genomic Island with Novel Regulatory and Metabolic Genes Melnyk, Ryan A.; Engelbrektson, Anna; Clark, Iain C. Applied and Environmental Microbiology, Vol. 77, Issue 20 https://doi.org/10.1128/AEM.05758-11	journal	August 2011
Ubiquity and Diversity of Dissimilatory (Per)chlorate-Reducing Bacteria Coates, John D.; Michaelidou, Urania; Bruce, Royce A. Applied and Environmental Microbiology, Vol. 65, Issue 12 https://doi.org/10.1128/AEM.65.12.5234-5241.1999	journal	December 1999
Sequencing and Transcriptional Analysis of the Chlorite Dismutase Gene of Dechloromonas agitata and Its Use as a Metabolic Probe Bender, Kelly S.; O'Connor, Susan M.; Chakraborty, Romy Applied and Environmental Microbiology, Vol. 68, Issue 10 https://doi.org/10.1128/AEM.68.10.4820-4826.2002	journal	October 2002
Growth of Dehalobacter and Dehalococcoides spp. during Degradation of Chlorinated Ethanes Grostern, A.; Edwards, E. A. Applied and Environmental Microbiology, Vol. 72, Issue 1 https://doi.org/10.1128/AEM.72.1.428-436.2006	journal	January 2006
Characterization of the Chlorate Reductase from Pseudomonas chloritidismutans Wolterink, Arthur F. W. M.; Schiltz, Emile; Hagedoorn, Peter-Leon Journal of Bacteriology, Vol. 185, Issue 10 https://doi.org/10.1128/JB.185.10.3210-3213.2003	journal	May 2003
Novel Mechanism for Scavenging of Hypochlorite Involving a Periplasmic Methionine-Rich Peptide and Methionine Sulfoxide Reductase Melnyk, Ryan A.; Youngblut, Matthew D.; Clark, Iain C. mBio, Vol. 6, Issue 3 https://doi.org/10.1128/mBio.00233-15	journal	May 2015
Structure and Evolution of Chlorate Reduction Composite Transposons Clark, Iain C.; Melnyk, Ryan A.; Engelbrektson, Anna mBio, Vol. 4, Issue 4 https://doi.org/10.1128/mBio.00379-13	journal	August 2013
Draft Genome Sequence of Comamonas aquatilis Strain LK (= CSUR P6418 = CECT 9772), Isolated from the Planarian Schmidtea mediterranea Kangale, Luis Johnson; Levasseur, Anthony; Raoult, Didier Microbiology Resource Announcements, Vol. 10, Issue 5 https://doi.org/10.1128/mra.00297-20	journal	February 2021
(Per)chlorate in Biology on Earth and Beyond Youngblut, Matthew D.; Wang, Ouwei; Barnum, Tyler P. Annual Review of Microbiology, Vol. 70, Issue 1 https://doi.org/10.1146/annurev-micro-102215-095406	journal	September 2016
Bacterial Responses to Reactive Chlorine Species Gray, Michael J.; Wholey, Wei-Yun; Jakob, Ursula Annual Review of Microbiology, Vol. 67, Issue 1 https://doi.org/10.1146/annurev-micro-102912-142520	journal	September 2013
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
The Perchlorate Reduction Genomic Island: Mechanisms and Pathways of Evolution by Horizontal Gene Transfer Melnyk, Ryan A.; Coates, John D. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-2011-5	journal	October 2015
The presence of nitrate dramatically changed the predominant microbial community in perchlorate degrading cultures under saline conditions Stepanov, Victor G.; Xiao, Yeyuan; Tran, Quyen BMC Microbiology, Vol. 14, Issue 1 https://doi.org/10.1186/s12866-014-0225-3	journal	September 2014
The presence of nitrate dramatically changed the predominant microbial community in perchlorate degrading cultures under saline conditions Stepanov, Victor G.; Xiao, Yeyuan; Tran, Quyen BioMed Central https://doi.org/10.14288/1.0223962	text	January 2014
Inhibition of microbial sulfate reduction in a flow-through column system by (per)chlorate treatment Engelbrektson, Anna; Hubbard, Christopher G.; Tom, Lauren M. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00315	journal	June 2014
Microbial Synthesis and Transformation of Inorganic and Organic Chlorine Compounds Atashgahi, Siavash; Liebensteiner, Martin G.; Janssen, Dick B. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03079	journal	December 2018
A total quasi-steady-state formulation of substrate uptake kinetics in complex networks and an example application to microbial litter decomposition Tang, J. Y.; Riley, W. J. Biogeosciences, Vol. 10, Issue 12 https://doi.org/10.5194/bg-10-8329-2013	journal	January 2013
The Perchlorate Reduction Genomic Island: Mechanisms and Pathways of Evolution by Horizontal Gene Transfer Melnyk, Ryan; Coates, John Figshare https://doi.org/10.6084/m9.figshare.c.3641789	collection	January 2015
Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015

Similar Records

Gaseous, chlorine-free chlorine dioxide for drinking water

Conference · Thu Oct 31 23:00:00 EST 1996 · OSTI ID:387288

Ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria

Journal Article · Tue Nov 30 23:00:00 EST 1999 · Applied and Environmental Microbiology · OSTI ID:20006176

Kinetics and mechanism of formation of chlorate ion from the hypochlorous acid/chlorite ion reaction at pH 6-10

Journal Article · Thu Feb 28 23:00:00 EST 1991 · Environmental Science and Technology; (USA) · OSTI ID:5486345

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Identification of a parasitic symbiosis between respiratory metabolisms in the biogeochemical chlorine cycle

Citation Formats

References (63)

Similar Records

Related Subjects