Characterizing Chemoautotrophy and Heterotrophy in Marine Archaea and Bacteria With Single-Cell Multi-isotope NanoSIP

Dekas, Anne E.; Parada, Alma E.; Mayali, Xavier; Fuhrman, Jed A.; Wollard, Jessica; Weber, Peter K.; Pett-Ridge, Jennifer

doi:10.3389/fmicb.2019.02682

Title: Characterizing Chemoautotrophy and Heterotrophy in Marine Archaea and Bacteria With Single-Cell Multi-isotope NanoSIP

Journal Article · 16 December 2019 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2019.02682 · OSTI ID:1579574

Dekas, Anne E.; Parada, Alma E.; Mayali, Xavier; Fuhrman, Jed A.; Wollard, Jessica; Weber, Peter K.; Pett-Ridge, Jennifer

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Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Laboratory Directed Research and Development (LDRD) Program; National Science Foundation (NSF); Gordon and Betty Moore Foundation

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1579574

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 10; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: Switzerland

Language:: English

References (66)

NanoSIP: NanoSIMS Applications for Microbial Biology Pett-Ridge, Jennifer; Weber, Peter K. Microbial Systems Biology https://doi.org/10.1007/978-1-61779-827-6_13	book	January 2012
ggplot2 Wickham, Hadley Use R! https://doi.org/10.1007/978-3-319-24277-4	book	January 2016
Ecophysiology of an Ammonia-Oxidizing Archaeon Adapted to Low-Salinity Habitats Mosier, Annika C.; Lund, Marie B.; Francis, Christopher A. Microbial Ecology, Vol. 64, Issue 4 https://doi.org/10.1007/s00248-012-0075-1	journal	May 2012
Origins of lipid biomarkers in Santa Monica Basin surface sediment: a case study using compound-specific Δ 14 C analysis Pearson, A.; McNichol, A. P.; Benitez-Nelson, B. C. Geochimica et Cosmochimica Acta, Vol. 65, Issue 18 https://doi.org/10.1016/S0016-7037(01)00657-3	journal	September 2001
Bicarbonate uptake by marine Crenarchaeota Wuchter, Cornelia; Schouten, Stefan; Boschker, Henricus T. S. FEMS Microbiology Letters, Vol. 219, Issue 2 https://doi.org/10.1016/S0378-1097(03)00060-0	journal	February 2003
Tracking activity and function of microorganisms by stable isotope probing of membrane lipids Wegener, Gunter; Kellermann, Matthias Y.; Elvert, Marcus Current Opinion in Biotechnology, Vol. 41 https://doi.org/10.1016/j.copbio.2016.04.022	journal	October 2016
Carbon Dioxide Assimilation in Heterotrophic Organisms Krebs, H. A. Nature, Vol. 147, Issue 3732 https://doi.org/10.1038/147560a0	journal	May 1941
Archaeal dominance in the mesopelagic zone of the Pacific Ocean Karner, Markus B.; DeLong, Edward F.; Karl, David M. Nature, Vol. 409, Issue 6819 https://doi.org/10.1038/35054051	journal	January 2001
Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides Popa, Radu; Weber, Peter K.; Pett-Ridge, Jennifer The ISME Journal, Vol. 1, Issue 4 https://doi.org/10.1038/ismej.2007.44	journal	July 2007
Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation Santoro, Alyson E.; Casciotti, Karen L. The ISME Journal, Vol. 5, Issue 11 https://doi.org/10.1038/ismej.2011.58	journal	May 2011
Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses Blazewicz, Steven J.; Barnard, Romain L.; Daly, Rebecca A. The ISME Journal, Vol. 7, Issue 11 https://doi.org/10.1038/ismej.2013.102	journal	July 2013
Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses Dekas, Anne E.; Connon, Stephanie A.; Chadwick, Grayson L. The ISME Journal, Vol. 10, Issue 3 https://doi.org/10.1038/ismej.2015.145	journal	September 2015
Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment Arandia-Gorostidi, Nestor; Weber, Peter K.; Alonso-Sáez, Laura The ISME Journal, Vol. 11, Issue 3 https://doi.org/10.1038/ismej.2016.156	journal	December 2016
Marine archaeal dynamics and interactions with the microbial community over 5 years from surface to seafloor Parada, Alma E.; Fuhrman, Jed A. The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.104	journal	July 2017
Isolation of an autotrophic ammonia-oxidizing marine archaeon Könneke, Martin; Bernhard, Anne E.; de la Torre, José R. Nature, Vol. 437, Issue 7058 https://doi.org/10.1038/nature03911	journal	September 2005
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life Parks, Donovan H.; Chuvochina, Maria; Waite, David W. Nature Biotechnology, Vol. 36, Issue 10 https://doi.org/10.1038/nbt.4229	journal	August 2018
Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea Li, Meng; Baker, Brett J.; Anantharaman, Karthik Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9933	journal	November 2015
QIIME allows analysis of high-throughput community sequencing data Caporaso, J. Gregory; Kuczynski, Justin; Stombaugh, Jesse Nature Methods, Vol. 7, Issue 5 https://doi.org/10.1038/nmeth.f.303	journal	April 2010
Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing: Methanotrophs in Movile Cave Hutchens, Elena; Radajewski, Stefan; Dumont, Marc G. Environmental Microbiology, Vol. 6, Issue 2 https://doi.org/10.1046/j.1462-2920.2003.00543.x	journal	December 2003
Quantifying archaeal community autotrophy in the mesopelagic ocean using natural radiocarbon Ingalls, A. E.; Shah, S. R.; Hansman, R. L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 17 https://doi.org/10.1073/pnas.0510157103	journal	April 2006
Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry Finzi-Hart, J. A.; Pett-Ridge, J.; Weber, P. K. Proceedings of the National Academy of Sciences, Vol. 106, Issue 15 https://doi.org/10.1073/pnas.0810547106	journal	March 2009
Role for urea in nitrification by polar marine Archaea Alonso-Saez, L.; Waller, A. S.; Mende, D. R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 44 https://doi.org/10.1073/pnas.1201914109	journal	October 2012
Autotrophy as a predominant mode of carbon fixation in anaerobic methane-oxidizing microbial communities Kellermann, M. Y.; Wegener, G.; Elvert, M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47 https://doi.org/10.1073/pnas.1208795109	journal	November 2012
Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation Qin, W.; Amin, S. A.; Martens-Habbena, W. Proceedings of the National Academy of Sciences, Vol. 111, Issue 34 https://doi.org/10.1073/pnas.1324115111	journal	August 2014
Ammonia-oxidizing archaea use the most energy-efficient aerobic pathway for CO2 fixation Konneke, M.; Schubert, D. M.; Brown, P. C. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1402028111	journal	May 2014
Tracking heavy water (D ₂ O) incorporation for identifying and sorting active microbial cells Berry, David; Mader, Esther; Lee, Tae Kwon Proceedings of the National Academy of Sciences, Vol. 112, Issue 2 https://doi.org/10.1073/pnas.1420406112	journal	December 2014
Search and clustering orders of magnitude faster than BLAST Edgar, Robert C. Bioinformatics, Vol. 26, Issue 19, p. 2460-2461 https://doi.org/10.1093/bioinformatics/btq461	journal	August 2010
Quality control and preprocessing of metagenomic datasets Schmieder, R.; Edwards, R. Bioinformatics, Vol. 27, Issue 6 https://doi.org/10.1093/bioinformatics/btr026	journal	January 2011
Discerning autotrophy, mixotrophy, and heterotrophy in marine TACK archaea from the North Atlantic Seyler, Lauren M.; McGuinness, Lora R.; Gilbert, Jack A. FEMS Microbiology Ecology https://doi.org/10.1093/femsec/fiy014	journal	January 2018
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0 Tamura, Koichiro; Stecher, Glen; Peterson, Daniel Molecular Biology and Evolution, Vol. 30, Issue 12 https://doi.org/10.1093/molbev/mst197	journal	October 2013
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Thompson, Julie D.; Higgins, Desmond G.; Gibson, Toby J. Nucleic Acids Research, Vol. 22, Issue 22, p. 4673-4680 https://doi.org/10.1093/nar/22.22.4673	journal	January 1994
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
Heavy water and ¹⁵ N labelling with NanoSIMS analysis reveals growth rate-dependent metabolic heterogeneity in chemostats : NanoSIMS analysis of metabolic diversity in chemostats Kopf, Sebastian H.; McGlynn, Shawn E.; Green-Saxena, Abigail Environmental Microbiology, Vol. 17, Issue 7 https://doi.org/10.1111/1462-2920.12752	journal	March 2015
Every base matters: assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples: Primers for marine microbiome studies Parada, Alma E.; Needham, David M.; Fuhrman, Jed A. Environmental Microbiology, Vol. 18, Issue 5 https://doi.org/10.1111/1462-2920.13023	journal	October 2015
Oxidation of urea-derived nitrogen by thaumarchaeota-dominated marine nitrifying communities: Oxidation of urea-derived nitrogen in the sea Tolar, Bradley B.; Wallsgrove, Natalie J.; Popp, Brian N. Environmental Microbiology, Vol. 19, Issue 12 https://doi.org/10.1111/1462-2920.13457	journal	August 2016
Genome and epigenome of a novel marine Thaumarchaeota strain suggest viral infection, phosphorothioation DNA modification and multiple restriction systems: Genome and epigenome of a new marine thaumarchaeon Ahlgren, Nathan A.; Chen, Yangyang; Needham, David M. Environmental Microbiology, Vol. 19, Issue 6 https://doi.org/10.1111/1462-2920.13768	journal	May 2017
Widespread nitrogen fixation in sediments from diverse deep‐sea sites of elevated carbon loading Dekas, Anne E.; Fike, David A.; Chadwick, Grayson L. Environmental Microbiology, Vol. 20, Issue 12 https://doi.org/10.1111/1462-2920.14342	journal	July 2018
Patterns of ¹⁵ N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS Orphan, Victoria J.; Turk, Kendra A.; Green, Abigail M. Environmental Microbiology, Vol. 11, Issue 7 https://doi.org/10.1111/j.1462-2920.2009.01903.x	journal	July 2009
Assessing sub-seafloor microbial activity by combined stable isotope probing with deuterated water and 13C-bicarbonate: Microbial carbon assimilation in the sub-seafloor Wegener, Gunter; Bausch, Marlene; Holler, Thomas Environmental Microbiology, Vol. 14, Issue 6 https://doi.org/10.1111/j.1462-2920.2012.02739.x	journal	April 2012
Taxon-specific C/N relative use efficiency for amino acids in an estuarine community Mayali, Xavier; Weber, Peter K.; Pett-Ridge, Jennifer FEMS Microbiology Ecology, Vol. 83, Issue 2 https://doi.org/10.1111/j.1574-6941.12000.x	journal	September 2012
Tracing the slow growth of anaerobic methane-oxidizing communities by 15N-labelling techniques: 15N-labelling of anaerobic methanotrophs KrÃ¼ger, Martin; Wolters, Heike; Gehre, Matthias FEMS Microbiology Ecology, Vol. 63, Issue 3 https://doi.org/10.1111/j.1574-6941.2007.00431.x	journal	March 2008
Deep-Sea Archaea Fix and Share Nitrogen in Methane-Consuming Microbial Consortia Dekas, A. E.; Poretsky, R. S.; Orphan, V. J. Science, Vol. 326, Issue 5951 https://doi.org/10.1126/science.1178223	journal	October 2009
Stable Isotope Ratios and Forensic Analysis of Microorganisms Kreuzer-Martin, H. W.; Jarman, K. H. Applied and Environmental Microbiology, Vol. 73, Issue 12 https://doi.org/10.1128/AEM.02906-06	journal	April 2007
Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Amann, R. I.; Binder, B. J.; Olson, R. J. Applied and Environmental Microbiology, Vol. 56, Issue 6 https://doi.org/10.1128/AEM.56.6.1919-1925.1990	journal	January 1990
Amine Oxidases of Marine Phytoplankton Palenik, Brian; Morel, François M. M. Applied and Environmental Microbiology, Vol. 57, Issue 8 https://doi.org/10.1128/AEM.57.8.2440-2443.1991	journal	January 1991
Relationship between the Intracellular Integrity and the Morphology of the Capsular Envelope in Attached and Free-Living Marine Bacteria. Heissenberger, A.; Leppard, G. G.; Herndl, G. J. Applied and environmental microbiology, Vol. 62, Issue 12 https://doi.org/10.1128/AEM.62.12.4521-4528.1996	journal	January 1996
Marine Planktonic Archaea Take Up Amino Acids Ouverney, C. C.; Fuhrman, J. A. Applied and Environmental Microbiology, Vol. 66, Issue 11 https://doi.org/10.1128/AEM.66.11.4829-4833.2000	journal	November 2000
Combining Catalyzed Reporter Deposition-Fluorescence In Situ Hybridization and Microautoradiography To Detect Substrate Utilization by Bacteria and Archaea in the Deep Ocean Teira, E.; Reinthaler, T.; Pernthaler, A. Applied and Environmental Microbiology, Vol. 70, Issue 7 https://doi.org/10.1128/AEM.70.7.4411-4414.2004	journal	July 2004
Isotope Labeling and Microautoradiography of Active Heterotrophic Bacteria on the Basis of Assimilation of 14CO2 Hesselsoe, M.; Nielsen, J. L.; Roslev, P. Applied and Environmental Microbiology, Vol. 71, Issue 2 https://doi.org/10.1128/AEM.71.2.646-655.2005	journal	February 2005
Contribution of Archaea to Total Prokaryotic Production in the Deep Atlantic Ocean Herndl, G. J.; Reinthaler, T.; Teira, E. Applied and Environmental Microbiology, Vol. 71, Issue 5 https://doi.org/10.1128/AEM.71.5.2303-2309.2005	journal	May 2005
Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition for the Identification of Marine Bacteria Pernthaler, A.; Pernthaler, J.; Amann, R. Applied and Environmental Microbiology, Vol. 68, Issue 6 https://doi.org/10.1128/aem.68.6.3094-3101.2002	journal	June 2002
Phylogenetically Novel Uncultured Microbial Cells Dominate Earth Microbiomes Lloyd, Karen G.; Steen, Andrew D.; Ladau, Joshua mSystems, Vol. 3, Issue 5 https://doi.org/10.1128/mSystems.00055-18	journal	September 2018
MAR-FISH—An Ecophysiological Approach to Link Phylogenetic Affiliation and In Situ Metabolic Activity of Microorganisms at a Single-Cell Resolution Okabe, Satoshi; Kindaichi, Tomonori; Ito, Tsukasa Microbes and Environments, Vol. 19, Issue 2 https://doi.org/10.1264/jsme2.19.83	journal	January 2004
Pathways of Carbon Assimilation and Ammonia Oxidation Suggested by Environmental Genomic Analyses of Marine Crenarchaeota Hallam, Steven J.; Mincer, Tracy J.; Schleper, Christa PLoS Biology, Vol. 4, Issue 4, Article No. e95 https://doi.org/10.1371/journal.pbio.0040095	journal	March 2006
Genome of a Low-Salinity Ammonia-Oxidizing Archaeon Determined by Single-Cell and Metagenomic Analysis Blainey, Paul C.; Mosier, Annika C.; Potanina, Anastasia PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016626	journal	February 2011
phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data McMurdie, Paul J.; Holmes, Susan PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061217	journal	April 2013
Genomic and Metabolic Diversity of Marine Group I Thaumarchaeota in the Mesopelagic of Two Subtropical Gyres Swan, Brandon K.; Chaffin, Mark D.; Martinez-Garcia, Manuel PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0095380	journal	April 2014
Extracellular amino acid oxidation by microplankton: a cross-ecosystem comparison Mulholland, Mr; Glibert, Pm; Berg, Gm Aquatic Microbial Ecology, Vol. 15 https://doi.org/10.3354/ame015141	journal	January 1998
Extracellular enzyme activity and uptake of carbon and nitrogen along an estuarine salinity and nutrient gradient Mulholland, Mr; Lee, C.; Glibert, Pm Marine Ecology Progress Series, Vol. 258 https://doi.org/10.3354/meps258003	journal	January 2003
Chemoautotrophic growth of ammonia-oxidizing Thaumarchaeota enriched from a pelagic redox gradient in the Baltic Sea Berg, Carlo; Listmann, Luisa; Vandieken, Verona Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00786	journal	January 2015
Phenotypic heterogeneity in metabolic traits among single cells of a rare bacterial species in its natural environment quantified with a combination of flow cell sorting and NanoSIMS Zimmermann, Matthias; Escrig, Stéphane; Hübschmann, Thomas Frontiers in Microbiology, Vol. 06 https://doi.org/10.3389/fmicb.2015.00243	journal	April 2015
Stable Isotope Phenotyping via Cluster Analysis of NanoSIMS Data As a Method for Characterizing Distinct Microbial Ecophysiologies and Sulfur-Cycling in the Environment Dawson, Katherine S.; Scheller, Silvan; Dillon, Jesse G. Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.00774	journal	May 2016
Bacterioplankton distribution and production in deep Pacific waters: Large-scale geographic variations and possible coupling with sinking particle fluxes Nagata, Toshi; Fukuda, Hideki; Fukuda, Rumi Limnology and Oceanography, Vol. 45, Issue 2 https://doi.org/10.4319/lo.2000.45.2.0426	journal	March 2000
Prokaryotic respiration and production in the meso- and bathypelagic realm of the eastern and western North Atlantic basin Reinthaler, Thomas; van Aken, Hendrik; Veth, Cornelis Limnology and Oceanography, Vol. 51, Issue 3 https://doi.org/10.4319/lo.2006.51.3.1262	journal	May 2006
Standing stocks and activity of Archaea and Bacteria in the western Arctic Ocean Kirchman, David L.; Elifantz, Hila; Dittel, Ana I. Limnology and Oceanography, Vol. 52, Issue 2 https://doi.org/10.4319/lo.2007.52.2.0495	journal	March 2007
Swarm: robust and fast clustering method for amplicon-based studies Mahé, Frédéric; Rognes, Torbjørn; Quince, Christopher PeerJ, Vol. 2 https://doi.org/10.7717/peerj.593	journal	January 2014

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