Underwater Application of Quantitative PCR on an Ocean Mooring

Preston, Christina M.; Harris, Adeline; Ryan, John P.; Roman, Brent; Marin III, Roman; Jensen, Scott; Everlove, Cheri; Birch, James; Dzenitis, John M.; Pargett, Douglas; Adachi, Masao; Turk, Kendra; Zehr, Jonathon P.; Scholin, Christopher A.

doi:10.1371/journal.pone.0022522

Underwater Application of Quantitative PCR on an Ocean Mooring

Journal Article · Mon Aug 01 04:00:00 EDT 2011 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0022522· OSTI ID:1627466

Preston, Christina M. ^[1]; Harris, Adeline ^[2]; Ryan, John P. ^[2]; Roman, Brent ^[2]; Marin III, Roman ^[2]; Jensen, Scott ^[2]; Everlove, Cheri ^[2]; Birch, James ^[2]; Dzenitis, John M. ^[3]; Pargett, Douglas ^[2]; Adachi, Masao ^[4]; Turk, Kendra ^[5]; Zehr, Jonathon P. ^[5]; Scholin, Christopher A. ^[2]

Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States); DOE/OSTI
Monterey Bay Aquarium Research Inst., Moss Landing, CA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Kochi Univ. (Japan). Lab. of Aquatic Environmental Science
Univ. of California, Santa Cruz, CA (United States). Dept. of Ocean Sciences and Earth and Marine Sciences

The Environmental Sample Processor (ESP) is a device that allows for the underwater, autonomous application of DNA and protein probe array technologies as a means to remotely identify and quantify, in situ, marine microorganisms and substances they produce. Here, we added functionality to the ESP through the development and incorporation of a module capable of solid-phase nucleic acid extraction and quantitative PCR (qPCR). Samples collected by the instrument were homogenized in a chaotropic buffer compatible with direct detection of ribosomal RNA (rRNA) and nucleic acid purification. From a single sample, both an rRNA community profile and select gene abundances were ascertained. To illustrate this functionality, we focused on bacterioplankton commonly found along the central coast of California and that are known to vary in accordance with different oceanic conditions. DNA probe arrays targeting rRNA revealed the presence of 16S rRNA indicative of marine crenarchaea, SAR11 and marine cyanobacteria; in parallel, qPCR was used to detect 16S rRNA genes from the former two groups and the large subunit RuBisCo gene (rbcL) from Synecchococcus. The PCR-enabled ESP was deployed on a coastal mooring in Monterey Bay for 28 days during the spring-summer upwelling season. The distributions of the targeted bacterioplankon groups were as expected, with the exception of an increase in abundance of marine crenarchaea in anomalous nitrate-rich, low-salinity waters. The unexpected co-occurrence demonstrated the utility of the ESP in detecting novel events relative to previously described distributions of particular bacterioplankton groups. The ESP can easily be configured to detect and enumerate genes and gene products from a wide range of organisms. This study demonstrated for the first time that gene abundances could be assessed autonomously, underwater in near real-time and referenced against prevailing chemical, physical and bulk biological conditions.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); David and Lucille Packard Foundation; National Science Foundation (NSF); Gordon and Betty Moore Foundation; National Aeronautics and Space Administration (NASA)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1627466

Report Number(s):: LLNL-JRNL--480573

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 8 Vol. 6; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (55)

Molecular Detection of Marine Invertebrate Larvae Goffredi, Shana K.; Jones, William J.; Scholin, Christopher A. Marine Biotechnology, Vol. 8, Issue 2 https://doi.org/10.1007/s10126-005-5016-2	journal	January 2006
Measurement of unbound bilirubin by the peroxidase test using Zone Fluidics Ahlfors, Charles E.; Marshall, Graham D.; Wolcott, Duane K. Clinica Chimica Acta, Vol. 365, Issue 1-2 https://doi.org/10.1016/j.cca.2005.07.030	journal	March 2006
Electrochemical detection of harmful algae and other microbial contaminants in coastal waters using hand-held biosensors LaGier, Michael J.; Fell, Jack W.; Goodwin, Kelly D. Marine Pollution Bulletin, Vol. 54, Issue 6 https://doi.org/10.1016/j.marpolbul.2006.12.017	journal	June 2007
Automated methods for multiplexed pathogen detection Straub, Timothy M.; Dockendorff, Brian P.; Quiñonez-Díaz, Maria D. Journal of Microbiological Methods, Vol. 62, Issue 3 https://doi.org/10.1016/j.mimet.2005.04.012	journal	September 2005
Sequential injection: a new concept for chemical sensors, process analysis and laboratory assays Ruzicka, Jaromir; Marshall, Graham D. Analytica Chimica Acta, Vol. 237 https://doi.org/10.1016/s0003-2670(00)83937-9	journal	January 1990
Nutrient dynamics in the deep blue sea Karl, David M. Trends in Microbiology, Vol. 10, Issue 9 https://doi.org/10.1016/s0966-842x(02)02430-7	journal	September 2002
A Reusable Flow-Through Polymerase Chain Reaction Instrument for the Continuous Monitoring of Infectious Biological Agents Belgrader, Phillip; Elkin, Christopher J.; Brown, Steven B. Analytical Chemistry, Vol. 75, Issue 14 https://doi.org/10.1021/ac034062u	journal	July 2003
Development of an Automated Sample Preparation Module for Environmental Monitoring of Biowarfare Agents Hindson, Benjamin J.; Brown, Steve B.; Marshall, Graham D. Analytical Chemistry, Vol. 76, Issue 13 https://doi.org/10.1021/ac035365r	journal	July 2004
Autonomous Detection of Aerosolized Biological Agents by Multiplexed Immunoassay with Polymerase Chain Reaction Confirmation Hindson, Benjamin J.; McBride, Mary T.; Makarewicz, Anthony J. Analytical Chemistry, Vol. 77, Issue 1 https://doi.org/10.1021/ac0489014	journal	January 2005
Relationship and Variation of qPCR and Culturable Enterococci Estimates in Ambient Surface Waters Are Predictable Whitman, Richard L.; Ge, Zhongfu; Nevers, Meredith B. Environmental Science & Technology, Vol. 44, Issue 13 https://doi.org/10.1021/es9028974	journal	July 2010
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
Metatranscriptomic analysis of autonomously collected and preserved marine bacterioplankton Ottesen, Elizabeth A.; Marin, Roman; Preston, Christina M. The ISME Journal, Vol. 5, Issue 12 https://doi.org/10.1038/ismej.2011.70	journal	June 2011
Microbial oceanography in a sea of opportunity Bowler, Chris; Karl, David M.; Colwell, Rita R. Nature, Vol. 459, Issue 7244 https://doi.org/10.1038/nature08056	journal	May 2009
Archaeal nitrification in the ocean Wuchter, C.; Abbas, B.; Coolen, M. J. L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 33 https://doi.org/10.1073/pnas.0600756103	journal	August 2006
Real time quantitative PCR. Heid, C. A.; Stevens, J.; Livak, K. J. Genome Research, Vol. 6, Issue 10, p. 986-994 https://doi.org/10.1101/gr.6.10.986	journal	October 1996
Quantitative distribution of presumptive archaeal and bacterial nitrifiers in Monterey Bay and the North Pacific Subtropical Gyre Mincer, Tracy J.; Church, Matthew J.; Taylor, Lance Trent Environmental Microbiology, Vol. 9, Issue 5 https://doi.org/10.1111/j.1462-2920.2007.01239.x	journal	May 2007
Near real-time, autonomous detection of marine bacterioplankton on a coastal mooring in Monterey Bay, California, using rRNA-targeted DNA probes Preston, Christina M.; Marin, Roman; Jensen, Scott D. Environmental Microbiology, Vol. 11, Issue 5 https://doi.org/10.1111/j.1462-2920.2009.01848.x	journal	May 2009
Changes in Benthic Denitrification, Nitrate Ammonification, and Anammox Process Rates and Nitrate and Nitrite Reductase Gene Abundances along an Estuarine Nutrient Gradient (the Colne Estuary, United Kingdom) Dong, L. F.; Smith, C. J.; Papaspyrou, S. Applied and Environmental Microbiology, Vol. 75, Issue 10 https://doi.org/10.1128/aem.02511-08	journal	March 2009
Quantitative Analysis of Small-Subunit rRNA Genes in Mixed Microbial Populations via 5'-Nuclease Assays Suzuki, M. T.; Taylor, L. T.; DeLong, E. F. Applied and Environmental Microbiology, Vol. 66, Issue 11, p. 4605-4614 https://doi.org/10.1128/aem.66.11.4605-4614.2000	journal	November 2000
Automated Purification and Suspension Array Detection of 16S rRNA from Soil and Sediment Extracts by Using Tunable Surface Microparticles Chandler, Darrell P.; Jarrell, Ann E. Applied and Environmental Microbiology, Vol. 70, Issue 5 https://doi.org/10.1128/aem.70.5.2621-2631.2004	journal	May 2004
Temporal Patterns of Nitrogenase Gene (nifH) Expression in the Oligotrophic North Pacific Ocean Church, Matthew J.; Short, Cindy M.; Jenkins, Bethany D. Applied and Environmental Microbiology, Vol. 71, Issue 9 https://doi.org/10.1128/aem.71.9.5362-5370.2005	journal	September 2005
Detection and enumeration of Heterosigma akashiwo and Fibrocapsa japonica (Raphidophyceae) using rRNA-targeted oligonucleotide probes Tyrrell, John V.; Bergquist, Patricia R.; Bergquist, Peter L. Phycologia, Vol. 40, Issue 5 https://doi.org/10.2216/i0031-8884-40-5-457.1	journal	September 2001
Molecular biology techniques and applications for ocean sensing Zehr, J. P.; Hewson, I.; Moisander, P. Ocean Science, Vol. 5, Issue 2 https://doi.org/10.5194/os-5-101-2009	journal	January 2009
Sequential injection: a new concept for chemical sensors, process analysis and laboratory assays Ruzicka, Jaromir; Marshall, Graham D. Analytica Chimica Acta, Vol. 237 https://doi.org/10.1016/S0003-2670(00)83937-9	journal	January 1990
Renewable microcolumns for automated DNA purification and flow-through amplification: from sediment samples through polymerase chain reaction Bruckner-Lea, Cynthia J.; Tsukuda, Toyoko; Dockendorff, Brian Analytica Chimica Acta, Vol. 469, Issue 1 https://doi.org/10.1016/S0003-2670(01)01438-6	journal	September 2002
Quantitative Analysis of nifH Genes and Transcripts from Aquatic Environments Short, Steven M.; Zehr, Jonathan P. Methods in Enzymology https://doi.org/10.1016/S0076-6879(05)97023-7	book	January 2005
Nutrient dynamics in the deep blue sea Karl, David M. Trends in Microbiology, Vol. 10, Issue 9 https://doi.org/10.1016/S0966-842X(02)02430-7	journal	September 2002
In situ ultraviolet spectrophotometry for high resolution and long-term monitoring of nitrate, bromide and bisulfide in the ocean Johnson, Kenneth S.; Coletti, Luke J. Deep Sea Research Part I: Oceanographic Research Papers, Vol. 49, Issue 7 https://doi.org/10.1016/S0967-0637(02)00020-1	journal	July 2002
Microfabricated flow-through device for DNA amplification—towards in situ gene analysis Fukuba, Tatsuhiro; Yamamoto, Takatoki; Naganuma, Takeshi Chemical Engineering Journal, Vol. 101, Issue 1-3 https://doi.org/10.1016/j.cej.2003.11.016	journal	August 2004
Interacting physical, chemical and biological forcing of phytoplankton thin-layer variability in Monterey Bay, California Ryan, John P.; McManus, Margaret A.; Sullivan, James M. Continental Shelf Research, Vol. 30, Issue 1 https://doi.org/10.1016/j.csr.2009.10.017	journal	January 2010
A handheld NASBA analyzer for the field detection and quantification of Karenia brevis Casper, Erica T.; Patterson, Stacey S.; Bhanushali, Pragnesh Harmful Algae, Vol. 6, Issue 1 https://doi.org/10.1016/j.hal.2006.11.001	journal	January 2007
Remote, subsurface detection of the algal toxin domoic acid onboard the Environmental Sample Processor: Assay development and field trials Doucette, Gregory J.; Mikulski, Christina M.; Jones, Kelly L. Harmful Algae, Vol. 8, Issue 6 https://doi.org/10.1016/j.hal.2009.04.006	journal	September 2009
Controlling a Robotic Marine Environmental Sampler with the Ruby Scripting Language Roman, B.; Scholin, C.; Jensen, S. Journal of the Association for Laboratory Automation, Vol. 12, Issue 1 https://doi.org/10.1016/j.jala.2006.07.013	journal	February 2007
Environmental Monitoring for Biological Threat Agents Using the Autonomous Pathogen Detection System with Multiplexed Polymerase Chain Reaction Regan, John F.; Makarewicz, Anthony J.; Hindson, Benjamin J. Analytical Chemistry, Vol. 80, Issue 19 https://doi.org/10.1021/ac801125x	journal	October 2008
The microbial ocean from genomes to biomes DeLong, Edward F. Nature, Vol. 459, Issue 7244 https://doi.org/10.1038/nature08059	journal	May 2009
Development of an automated DNA purification module using a micro-fabricated pillar chip Hindson, Benjamin J.; Gutierrez, Dora M.; Ness, Kevin D. The Analyst, Vol. 133, Issue 2 https://doi.org/10.1039/B713332D	journal	January 2008
Activity, abundance and diversity of nitrifying archaea and bacteria in the central California Current: Nitrification in the central California Current Santoro, Alyson E.; Casciotti, Karen L.; Francis, Christopher A. Environmental Microbiology, Vol. 12, Issue 7 https://doi.org/10.1111/j.1462-2920.2010.02205.x	journal	March 2010
A robotic molecular method for in situ detection of marine invertebrate larvae Jones, William J.; Preston, Christina M.; Marin Iii, Roman Molecular Ecology Resources, Vol. 8, Issue 3 https://doi.org/10.1111/j.1471-8286.2007.02021.x	journal	May 2008
Molecular detection of the brevetoxin-producing dinoflagellate Karenia brevis and closely related species using rRNA-targeted probes and a semiautomated sandwich hybridization assay ¹ Haywood, Allison J.; Scholin, Christopher A.; Marin, Roman Journal of Phycology, Vol. 43, Issue 6 https://doi.org/10.1111/j.1529-8817.2007.00407.x	journal	December 2007
Variations in spatial and temporal distribution of Archaea in the North Sea in relation to environmental variables: Marine Archaea in the North Sea Herfort, Lydie; Schouten, Stefan; Abbas, Ben FEMS Microbiology Ecology, Vol. 62, Issue 3 https://doi.org/10.1111/j.1574-6941.2007.00397.x	journal	December 2007
Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology: Application of Q-PCR in microbial ecology Smith, Cindy J.; Osborn, A. Mark FEMS Microbiology Ecology, Vol. 67, Issue 1 https://doi.org/10.1111/j.1574-6941.2008.00629.x	journal	January 2009
Changes in Benthic Denitrification, Nitrate Ammonification, and Anammox Process Rates and Nitrate and Nitrite Reductase Gene Abundances along an Estuarine Nutrient Gradient (the Colne Estuary, United Kingdom) Dong, L. F.; Smith, C. J.; Papaspyrou, S. Applied and Environmental Microbiology, Vol. 75, Issue 10 https://doi.org/10.1128/AEM.02511-08	journal	March 2009
Quantitative Analysis of Small-Subunit rRNA Genes in Mixed Microbial Populations via 5'-Nuclease Assays Suzuki, M. T.; Taylor, L. T.; DeLong, E. F. Applied and Environmental Microbiology, Vol. 66, Issue 11, p. 4605-4614 https://doi.org/10.1128/AEM.66.11.4605-4614.2000	journal	November 2000
Automated Purification and Suspension Array Detection of 16S rRNA from Soil and Sediment Extracts by Using Tunable Surface Microparticles Chandler, Darrell P.; Jarrell, Ann E. Applied and Environmental Microbiology, Vol. 70, Issue 5 https://doi.org/10.1128/AEM.70.5.2621-2631.2004	journal	May 2004
Development of a Rapid Assay for Determining the Relative Abundance of Bacteria Rowan, Arlene K.; Davenport, Russell J.; Snape, Jason R. Applied and Environmental Microbiology, Vol. 71, Issue 12 https://doi.org/10.1128/AEM.71.12.8481-8490.2005	journal	December 2005
Temporal Patterns of Nitrogenase Gene (nifH) Expression in the Oligotrophic North Pacific Ocean Church, Matthew J.; Short, Cindy M.; Jenkins, Bethany D. Applied and Environmental Microbiology, Vol. 71, Issue 9 https://doi.org/10.1128/AEM.71.9.5362-5370.2005	journal	September 2005
Quantitative mapping of bacterioplankton populations in seawater: field tests across an upwelling plume in Monterey Bay Suzuki, Mt; Preston, Cm; Chavez, Fp Aquatic Microbial Ecology, Vol. 24 https://doi.org/10.3354/ame024117	journal	January 2001
Harmful phytoplankton ecology studies using an autonomous molecular analytical and ocean observing network Ryan, J.; Greenfield, D.; Marin, R. Iii Limnology and Oceanography, Vol. 56, Issue 4 https://doi.org/10.4319/lo.2011.56.4.1255	journal	May 2011
Optimization of DNA extraction for quantitative marine bacterioplankton community analysis: DNA extraction from bacterioplankton Boström, Kjärstin H.; Simu, Karin; Hagström, Åke Limnology and Oceanography: Methods, Vol. 2, Issue 11 https://doi.org/10.4319/lom.2004.2.365	journal	November 2004
Application of environmental sample processor (ESP) methodology for quantifying Pseudo-nitzschia australis using ribosomal RNA-targeted probes in sandwich and fluorescent in situ hybridization formats: Application of the ESP Greenfield, Dianne I.; Marin, Roman; Jensen, Scott Limnology and Oceanography: Methods, Vol. 4, Issue 11 https://doi.org/10.4319/lom.2006.4.426	journal	November 2006
Field applications of the second-generation Environmental Sample Processor (ESP) for remote detection of harmful algae: 2006-2007: Field applications of the ESP: 2006-2007 Greenfield, Dianne I.; Marin, Roman; Doucette, Gregory J. Limnology and Oceanography: Methods, Vol. 6, Issue 12 https://doi.org/10.4319/lom.2008.6.667	journal	December 2008
Mobile autonomous process sampling within coastal ocean observing systems: Mobile Autonomous Process Sampling (MAPS) Ryan, J. P.; Johnson, S. B.; Sherman, A. Limnology and Oceanography: Methods, Vol. 8, Issue 8 https://doi.org/10.4319/lom.2010.8.394	journal	August 2010
What are "ecogenomic sensors?" A review and thoughts for the future Scholin, C. A. Ocean Science, Vol. 6, Issue 1 https://doi.org/10.5194/os-6-51-2010	journal	January 2010
Building the Long-Term Picture: The U.S. JGOFS Time-Series Programs Karl, David; Dore, John; Lukas, Roger Oceanography, Vol. 14, Issue 4 https://doi.org/10.5670/oceanog.2001.02	journal	January 2001
Remote Detection of Marine Microbes, Small Invertebrates, Harmful Algae, and Biotoxins using the Environmental Sample Processor (ESP) Scholin, Christopher; Doucette, Gregory; Jensen, Scott Oceanography, Vol. 22, Issue 2 https://doi.org/10.5670/oceanog.2009.46	journal	June 2009

Cited By (19)

Outbreak of coral-eating Crown-of-Thorns creates continuous cloud of larvae over 320 km of the Great Barrier Reef Uthicke, S.; Doyle, J.; Duggan, S. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep16885	journal	November 2015
Capturing Early Changes in the Marine Bacterial Community as a Result of Crude Oil Pollution in a Mesocosm Experiment Krolicka, Adriana; Boccadoro, Catherine; Nilsen, Mari Mæland Microbes and Environments, Vol. 32, Issue 4 https://doi.org/10.1264/jsme2.me17082	journal	January 2017
Salty sensors, fresh ideas: The use of molecular and imaging sensors in understanding plankton dynamics across marine and freshwater ecosystems Spanbauer, Trisha Lyn; Briseño‐Avena, Christian; Pitz, Kathleen Johnson Limnology and Oceanography Letters, Vol. 5, Issue 2 https://doi.org/10.1002/lol2.10128	journal	November 2019
Quantifying larvae of the coralivorous seastar Acanthaster cf. solaris on the Great Barrier Reef using qPCR Doyle, Jason R.; McKinnon, A. David; Uthicke, Sven Marine Biology, Vol. 164, Issue 8 https://doi.org/10.1007/s00227-017-3206-x	journal	August 2017
The ecology of environmental DNA and implications for conservation genetics Barnes, Matthew A.; Turner, Cameron R. Conservation Genetics, Vol. 17, Issue 1 https://doi.org/10.1007/s10592-015-0775-4	journal	September 2015
Ecogenomic sensor reveals controls on N2-fixing microorganisms in the North Pacific Ocean Robidart, Julie C.; Church, Matthew J.; Ryan, John P. The ISME Journal, Vol. 8, Issue 6 https://doi.org/10.1038/ismej.2013.244	journal	January 2014
Differential contributions of archaeal ammonia oxidizer ecotypes to nitrification in coastal surface waters Smith, Jason M.; Casciotti, Karen L.; Chavez, Francisco P. The ISME Journal, Vol. 8, Issue 8 https://doi.org/10.1038/ismej.2014.11	journal	February 2014
Single-taxon field measurements of bacterial gene regulation controlling DMSP fate Varaljay, Vanessa A.; Robidart, Julie; Preston, Christina M. The ISME Journal, Vol. 9, Issue 7 https://doi.org/10.1038/ismej.2015.23	journal	February 2015
Molecular genetic tools for environmental monitoring of New Zealand's aquatic habitats, past, present and the future Wood, Sa; Smith, Kf; Banks, Jc New Zealand Journal of Marine and Freshwater Research, Vol. 47, Issue 1 https://doi.org/10.1080/00288330.2012.745885	journal	March 2013
Functional gene surveys from ocean drilling expeditions - a review and perspective Lever, Mark A. FEMS Microbiology Ecology, Vol. 84, Issue 1 https://doi.org/10.1111/1574-6941.12051	journal	January 2013
Seasonality in Ocean Microbial Communities Giovannoni, S. J.; Vergin, K. L. Science, Vol. 335, Issue 6069 https://doi.org/10.1126/science.1198078	journal	February 2012
Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages Ottesen, E. A.; Young, C. R.; Gifford, S. M. Science, Vol. 345, Issue 6193 https://doi.org/10.1126/science.1252476	journal	July 2014
Development of an autonomous biosampler to capture in situ aquatic microbiomes Ribeiro, Hugo; Martins, Alfredo; Gonçalves, Marco PLOS ONE, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pone.0216882	journal	May 2019
Advancing Observation of Ocean Biogeochemistry, Biology, and Ecosystems With Cost-Effective in situ Sensing Technologies. Wang, Zhaohui Aleck; Moustahfid, Hassan; Mueller, Amy V. UNESCO/IOC https://doi.org/10.25607/obp-975	journalarticle	January 2019
In situ Autonomous Acquisition and Preservation of Marine Environmental DNA Using an Autonomous Underwater Vehicle Yamahara, Kevan M.; Preston, Christina M.; Birch, James Frontiers in Marine Science, Vol. 6 https://doi.org/10.3389/fmars.2019.00373	journal	July 2019
Advancing Observation of Ocean Biogeochemistry, Biology, and Ecosystems With Cost-Effective in situ Sensing Technologies Wang, Zhaohui Aleck; Moustahfid, Hassan; Mueller, Amy V. Frontiers in Marine Science, Vol. 6 https://doi.org/10.3389/fmars.2019.00519	journal	September 2019
Molecular Techniques for the Detection of Organisms in Aquatic Environments, with Emphasis on Harmful Algal Bloom Species Medlin, Linda; Orozco, Jahir Sensors, Vol. 17, Issue 5 https://doi.org/10.3390/s17051184	journal	May 2017
Distribution and drivers of symbiotic and free-living diazotrophic cyanobacteria in the western tropical South Pacific Stenegren, Marcus; Caputo, Andrea; Berg, Carlo Biogeosciences, Vol. 15, Issue 5 https://doi.org/10.5194/bg-15-1559-2018	journal	January 2018
Distribution and drivers of symbiotic and free-living diazotrophic cyanobacteria in the Western Tropical South Pacific Stenegren, Marcus; Caputo, Andrea; Berg, Carlo Biogeosciences Discuss https://doi.org/10.5194/bg-2017-63	posted_content	March 2017

Similar Records

Diversity and depth-specific distribution of SAR11 cluster rRNA genes from marine planktonic bacteria

Journal Article · Tue Dec 31 23:00:00 EST 1996 · Applied and Environmental Microbiology · OSTI ID:530722

Normalized Quantitative PCR Measurements as Predictors for Ethene Formation at Sites Impacted with Chlorinated Ethenes

Journal Article · Fri Oct 26 00:00:00 EDT 2018 · Environmental Science and Technology · OSTI ID:1545203

A robust PCR primer design platform applied to the detection of Acidobacteria Group 1 in soil

Journal Article · Tue Mar 20 00:00:00 EDT 2012 · Nucleic Acids Research · OSTI ID:1625503

Related Subjects

54 ENVIRONMENTAL SCIENCES
Science & Technology - Other Topics

Underwater Application of Quantitative PCR on an Ocean Mooring

Citation Formats

References (55)

Cited By (19)

Similar Records

Related Subjects