Oceanography The Official Magazine of
The Oceanography Society
Volume 30 Issue 04

View Issue TOC
Volume 30, No. 4
Pages 100 - 113

OpenAccess

The Quest to Develop Ecogenomic Sensors: A 25-Year History of the Environmental Sample Processor (ESP) as a Case Study

By Christopher A. Scholin , James Birch, Scott Jensen, Roman Marin III, Eugene Massion, Douglas Pargett, Christina Preston, Brent Roman, and William Ussler III 
Jump to
Article Abstract Citation References Copyright & Usage
Article Abstract

Roughly 25 years ago, “ecogenomic sensors” were conceived of as autonomous devices that would be used to apply molecular analytical techniques below the sea surface as one part of a futuristic, integrated ocean observing system. The Environmental Sample Processor (ESP) was built to address that idea—an instrument to help define both the technological and operational elements that underlie the eco­genomic sensor concept. Over time, the ESP emerged as a working example of that class of instrument, enabling the application of DNA probe and protein arrays as well as use of the quantitative polymerase chain reaction (qPCR) technique to assess the presence and abundance of a wide range of organisms, specific genes, and metabolites. The ESP is also used to preserve samples for a variety of laboratory tests not yet possible to carry out in situ (e.g., DNA sequencing). The instrument has been deployed on a variety of platforms, including coastal moorings, piers, an open ocean drifter, research vessels, a shallow water benthic lander, and a 4,000 m rated “elevator” designed for use on deep-sea cabled observatories. A new version of the ESP is currently being developed for use aboard an autonomous underwater vehicle. This article traces the evolution of the ESP from its conception to present-day status.

Citation

Scholin, C.A., J. Birch, S. Jensen, R. Marin III, E. Massion, D. Pargett, C. Preston, B. Roman, and W. Ussler III. 2017. The quest to develop ecogenomic sensors: A 25-Year history of the Environmental Sample Processor (ESP) as a case study. Oceanography 30(4):100–113, https://doi.org/10.5670/oceanog.2017.427.

References

Amann, R.I., B.J. Binder, R.J. Olson, S.W. Chisholm, R. Devereux, and D.A. Stahl. 1990. Combination of 16S ribosomal-RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial populations. Applied and Environmental Microbiology 56:1,919–1,925.

Andruszkiewicz, E.A., H.A. Starks, F.P. Chavez, L.M. Sassoubre, B.A. Block, and A.B. Boehm. 2017. Biomonitoring of marine vertebrates in Monterey Bay using eDNA metabarcoding. PLOS One 12(4):e0176343, https://doi.org/10.1371/journal.pone.0176343.

Aylward, F.O., J.M. Eppley, J.M. Smith, F.P. Chavez, C.A. Scholin, and E.F. DeLong. 2015. Microbial community transcriptional networks are conserved in three domains at ocean basin scales. Proceedings of the National Academy of Sciences of the United States of America 112:5,433–5,448, https://doi.org/​10.1073/pnas.1502883112.

Babin, M., J.J. Cullen, C.S. Roesler, P.L. Donaghay, G.J. Doucette, M. Kahru, M.R. Lewis, C.A. Scholin, M.E. Sieracki, and H.M. Sosik. 2005. New approaches and technologies for observing harmful algal blooms. Oceanography 18(2):210–227, https://doi.org/10.5670/oceanog.2005.55.

Bowers, H.A., R. Marin III, J.A. Birch, C.A. Scholin, and G.J. Doucette. 2016. Recovery and identification of Pseudo-nitzschia frustules from natural samples acquired using the Environmental Sample Processor (ESP). Journal of Phycology 52:135–140, https://doi.org/10.1111/jpy.12369.

Brewer, P.G., E.T. Peltzer, P.M. Walz, and W.J. Kirkwood. 2017. Creating the art of deep-sea experimental chemistry with MBARI ROVs. Oceanography 30(4):48–59, https://doi.org/​10.5670/oceanog.2017.423.

Chavez, F.P., J.T. Pennington, R.P. Michisaki, M. Blum, G.M. Chavez, J. Friederich, B. Jones, R. Herlien, B. Kieft, B. Hobson, and others. 2017. Climate variability and change: Response of a coastal ocean ecosystem. Oceanography 30(4):128–145, https://doi.org/10.5670/oceanog.2017.429.

Chisholm, S.W., R.J. Olson, E.R. Zettler, R. Goericke, J.B. Waterbury, and N.A. Welschmeyer. 1988. A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334:340–343, https://doi.org/10.1038/334340a0.

Church, M.J., C.M. Short, B.D. Jenkins, D.M. Karl, and J.P. Zehr. 2005. Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Applied and Environmental Microbiology 71:5,362–5,370; https://doi.org/​10.1128/AEM.71.9.5362-5370.2005.

DeLong, E.F. 1992. Archaea in coastal marine environments. Proceedings of the National Academy of Sciences of the United States of America 89:5,685–5,689, https://doi.org/10.1073/pnas.89.12.5685.

DeLong, E.F., G.S. Wickham, and N.R. Pace. 1989. Phylogenetic stains: Ribosomal RNA-based probes for the identification of single cells. Science 243:1,360–1,363, https://doi.org/10.1126/science.2466341.

Doucette, G.J., C.M. Mikulski, K.L. Jones, K.L. King, D.I. Greenfield, R. Marin III, S. Jensen, B. Roman, C.T. Elliott, and C.A. Scholin. 2009. Remote, subsurface detection of the algal toxin domoic acid onboard the Environmental Sample Processor: Assay development and field trials. Harmful Algae 8:880–888, https://doi.org/10.1016/j.hal.​2009.04.006.

Dyson, N.J. 1991. Immobilization of nucleic acids and hybridization analysis. Pp. 111–156 in Essential Molecular Biology: A Practical Approach, vol. 2. T.A. Brown, ed., Oxford University Press.

Field, K.G., G.J. Olsen, D.J. Lane, S.J. Giovannoni, M.T. Ghiselin, E.C. Raff, N.R. Pace, and R.A. Raff. 1988. Molecular phylogeny of the animal kingdom based on 18S ribosomal RNA sequences. Science 239:748–753, https://doi.org/10.1126/science.3277277.

Giovannoni, S.J., E.F. DeLong, G.J. Olsen, and N.R. Pace. 1988. Phylogenetic group-​​specific nucleic acid probes for identification of single microbial cells. Journal of Bacteriology 170:720–726, https://doi.org/​10.1128/jb.170.2.720-726.1988.

Giovannoni, S.J., E.F. DeLong, T.M. Schmidt, and N.R. Pace. 1990. Tangential flow filtration and preliminary phylogenetic analysis of marine picoplankton. Applied and Environmental Microbiology 56:2,572–2,575.

Goffredi, S.K., W.J. Jones, C.A. Scholin, R. Marin III, and R.C. Vrijenhoek. 2006. Molecular detection of marine larvae. Marine Biotechnology 8:149–160, https://doi.org/10.1007/s10126-005-5016-2.

Greenfield, D., R. Marin III, G.J. Doucette, C. Mikulski, S. Jensen, B. Roman, N. Alvarado, and C.A. Scholin. 2008. Field applications of the second-generation Environmental Sample Processor (ESP) for remote detection of harmful algae: 2006–2007. Limnology and Oceanography: Methods 6:667–679, https://doi.org/10.4319/lom.2008.6.667.

Greenfield, D.I., R. Marin III, S. Jensen, E. Massion, B. Roman, J. Feldman, and C.A. Scholin. 2006. Application of the Environmental Sample Processor (ESP) methodology for quantifying Pseudo-nitzschia australis using ribosomal RNA-targeted probes in sandwich and fluorescent in situ hybridization formats. Limnology and Oceanography: Methods 4:426–435, https://doi.org/10.4319/lom.2006.4.426.

Guidi, L., P.H.R Calil, S. Duhamel, K.M. Björkman, S.C. Doney, G.A. Jackson, B. Li, M.J. Church, S. Tozzi, Z.S. Kolber, and others. 2012. Does eddy-eddy interaction control surface phytoplankton distribution and carbon export in the North Pacific Subtropical Gyre? Journal of Geophysical Research 117, G02024, https://doi.org/​10.1029/​2012JG001984.

Haywood, A.J., C.A. Scholin, R. Marin III, K.A. Steidinger, C.A. Heil and J. Ray. 2007. Molecular detection of the brevetoxin-producing dinoflagellate Karenia brevis (Dinophyceae) and closely related species using ribosomal RNA probes and a semi-automated sandwich hybridization assay. Journal of Phycology 43:1,271–1,286, https://doi.org/10.1111/j.1529-8817.2007.00407.x.

Herfort, L., C. Seaton, M. Wilkin, B. Roman, C. Preston, R. Marin III, K. Seitz, M. Smith, V. Haynes, C. Scholin, A. Baptista, and H. Simon. 2016. Use of continuous, real-time observations and model simulations to achieve autonomous, adaptive sampling of microbial processes with a robotic sampler. Limnology and Oceanography: Methods 14:50–67, https://doi.org/​10.1002/lom3.10069.

Hobson, B.W., J.G. Bellingham, B. Kieft, R. McEwen, M. Godin, and Y. Zhang. 2012. Tethys-class long range AUVs: Extending the endurance of propeller-driven cruising AUVs from days to weeks. Pp. 1–8 in Autonomous Underwater Vehicles (AUV), 2012 IEEE/OES. Proceedings of September 24–27, 2012, meeting in Southampton, UK, https://doi.org/​10.1109/AUV.2012.6380735.

Jones, W.J., C. Preston, R. Marin III, C. Scholin, and R. Vrijenhoek. 2007. A robotic molecular method for in situ detection of marine invertebrate larvae. Molecular Ecology Resources 8:540–550, https://doi.org/10.1111/j.1471-8286.2007.02021.x.

Kelly, R.P., J.A. Port, K.M. Yamahara, and L.B. Crowder. 2014. Using environmental DNA to census marine fishes in a large mesocosm. PLoS ONE 9(1):e86175, https://doi.org/10.1371/journal.pone.0086175.

Marin, R. III, and C. Scholin. 2010. Sandwich hybridization. Chapter 12 in Microscopic and Molecular Methods for Quantitative Phytoplankton Analysis. B. Karlson, C. Cusack, and E. Bresnan, eds, IOC Manuals and Guides, no. 55, (IOC/2010/MG/55) Paris, UNESCO.

Mikulski, C.M., Y.T. Park, K.L. Jones, C.K. Lee, W.A. Lim, C.A. Scholin, and G.J. Doucette. 2008. Development and filed application of rRNA-​​targeted probes for the detection of Cochlodinium ploykrikoides in Korean coastal waters using whole cell and sandwich hybridization formats. Harmful Algae 7:347–359, https://doi.org/10.1016/​j.hal.2007.12.015.

Miller, P.E., and C.A. Scholin. 1998. Identification and enumeration of cultured and wild Pseudo-nitzschia (Bacillariophyceae) using species-​specific LSU rRNA-targeted fluorescent probes and filter-based whole cell hybridization. Journal of Phycology 34:371–382, https://doi.org/​10.1046/j.1529-8817.1998.340371.x.

Miller, P.E., and C.A. Scholin. 2000. On detection of Pseudo-nitzschia species using rRNA-​targeted probes: Sample fixation and stability. Journal of Phycology 36:238–250, https://doi.org/​10.1046/j.1529-8817.2000.99041.x.

Olins, H.C., D.R. Rogers, C. Preston, W. Ussler III, D. Pargett, S. Jensen, B. Roman, J.M. Birch, C.A. Scholin, M.F. Haroon, and P.R. Girguis. 2017. Co-registered geochemistry and metatranscriptomics reveal unexpected distributions of microbial activity within a hydrothermal vent field. Frontiers in Microbiology 8:1042, https://doi.org/10.3389/fmicb.2017.01042.

Olsen, G.J., D.J. Lane, S.J. Giovannoni, D.A. Stahl, and N.R. Pace. 1986. Microbial ecology and evolution: A ribosomal RNA approach. Annual Review of Microbiology 40:337–365, https://doi.org/10.1146/annurev.mi.40.100186.002005.

Ottesen, E.A., C.R. Young, J.M. Eppley, J.P. Ryan, F.P. Chavez, C.A. Scholin, and E.F. DeLong. 2013. Pattern and synchrony of gene expression among sympatric marine microbial populations. Proceedings of the National Academy of Sciences of the United States of America 110:E488–497, https://doi.org/10.1073/pnas.1222099110.

Ottesen, E.A., C.R. Young, S.M. Gifford, J.M. Eppley, R. Marin III, S.C. Schuster, C.A. Scholin, and E.F. DeLong. 2014. Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science 345:207–212, https://doi.org/​​10.1126/science.1252476.

Pace, N.R., D.A. Stahl, D.J. Lane, and G.J. Olsen. 1986. The analysis of natural microbial populations by ribosomal RNA sequences. Pp. 1–55 in Advances in Microbial Ecology, vol. 9. K.C. Marshall, ed., https://doi.org/10.1007/978-1-4757-0611-6_1.

Packard, D. 1989. Welcoming remarks to The Oceanography Society at its inaugural meeting. Oceanography 2(2):46-47, https://doi.org/10.5670/oceanog.1989.15.

Paul, J., C. Scholin, G. van den Engh, and M.J. Perry. 2007. In situ instrumentation. Oceanography 20(2):70–78, https:/doi.org/​10.5670/oceanog.2007.50.

Port, J.A., J.L. O’Donnell, O.C. Romero-Maraccini, P.R. Leary, S.Y. Litvin, K.J. Nickols, K.M. Yamahara, and R.P. Kelly. 2016. Assessing vertebrate biodiversity in a kelp forest ecosystem using environmental DNA. Molecular Ecology 25:527–541, https://doi.org/​​10.1111/​mec.13481.

Preston, C.M., A. Harris, J.P. Ryan, B. Roman, R. Marin III, S. Jensen, C. Everlove, J. Birch, J.M. Dzenitis, D. Pargett, and others. 2011. Underwater application of quantitative PCR on an ocean mooring. PLoS ONE 6(8):e22522, https://doi.org/​10.1371/​journal.pone.0022522.

Preston, C., R. Marin III, S. Jenson, J. Feldman, E. Massion, E. DeLong, M. Suzuki, K. Wheeler, D. Cline, N. Alvarado, and C. Scholin. 2009. Near real-time, autonomous detection of marine bacterioplankton on a coastal mooring in Monterey Bay, California, using rRNA-targeted DNA probes. Environmental Microbiology 11:1,168–1,180, https://doi.org/10.1111/j.1462-2920.2009.01848.x.

Robidart, J.C., M.J. Church, J.P. Ryan, F. Ascani, S.T. Wilson, D. Bombar, R. Marin III, K.J. Richards, D.M. Karl, C.A. Scholin, and J.P. Zehr. 2014. Ecogenomic sensor reveals controls on N2-fixing microorganisms in the North Pacific Ocean. The ISME Journal 8:1,175–1,185, https://doi.org/10.1038/ismej.2013.244.

Robidart, J.C., C.M. Preston, R.W. Paerl, K.A. Turk, A.C. Mosier, C.A. Francis, C.A. Scholin, and J.P. Zehr. 2012. Seasonal dynamics of Synechococcus and Thaumarchaeal microbial populations in Monterey Bay resolved in real time with remote in situ instrumentation. The ISME Journal 6:513–523, https://doi.org/10.1038/ismej.2011.127.

Robison, B.H., K.R. Reisenbichler, and R.E. Sherlock. 2017. The coevolution of midwater research and ROV technology at MBARI. Oceanography 30(4):26–37, https://doi.org/​10.5670/oceanog.2017.421.

Roman, B., C. Scholin, S. Jensen, E. Massion, R. Marin III, C. Preston, D. Greenfield, W. Jones, and K. Wheeler. 2007. Controlling a robotic marine water sampler with the Ruby Scripting Language. Journal of American Laboratory Automation 12:56–61, https://doi.org/10.1016/​j.jala.2006.07.013.

Ryan, J., D. Greenfield, R. Marin III, C. Preston, B. Roman, S. Jensen, D. Pargett, J. Birch, C. Mikulski, G. Doucette, and C. Scholin. 2011. Harmful phytoplankton ecology studies using an autonomous molecular analytical and ocean observing network. Limnology and Oceanography 56:1,255–1,272, https://doi.org/​10.4319/lo.2011.56.4.1255.

Ryan, J.P., R.M. Kudela, J.M. Birch, M. Blum, H.A. Bowers, F.P. Chavez, G.L. Doucette, K. Hayashi, R. Marin III, C.M. Mikulski, and others. 2017. Causality of an extreme harmful algal bloom in Monterey Bay, California, during the 2014–2016 northeast Pacific warm anomaly. Geophysical Research Letters 44:5,571–5,579, https://doi.org/​10.1002/​2017GL072637.

Sakamoto, C.M., K.S. Johnson, L.J. Coletti, T.L. Maurer, G. Massion, J.T. Pennington, J.N. Plant, H.W. Jannasch, and F.P. Chavez. 2017. Hourly in situ nitrate on a coastal mooring: A 15-year record and insights into new production. Oceanography 30(4):114–127, https://doi.org/​10.5670/oceanog.2017.428.

Schmidt, T.M., E.F. DeLong, and N.R. Pace. 1991. Analysis of a marine picoplankton community using 16S rRNA gene cloning and sequencing. Journal of Bacteriology 173:4,371–4,378, https://doi.org/​10.1128/jb.173.14.4371-4378.1991.

Scholin, C.A. 2013. Ecogenomic sensors. Pp. 690–700 in Encyclopedia of Biodiversity, 2nd ed., vol. 2. S.A. Levin, ed., Academic Press, Waltham, MA.

Scholin, C.A., and D.M. Anderson. 1994. Identification of group and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae): Part I. RFLP analysis of SSU rRNA genes. Journal of Phycology 30:744–754, https://doi.org/​10.1111/​j.0022-3646.1994.00744.x.

Scholin, C.A., and D.M. Anderson. 1998. Detection and quantification of HAB species using antibody and DNA probes: Progress to date and future research objectives. Pp. 253–257 in Harmful Algae. B. Regura, J. Blanko, M.L. Fernandez, and T. Wyatt, eds, Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO.

Scholin, C.A., K.R. Buck, T. Britschgi, J. Cangelosi, and F.P. Chavez. 1996. Identification of Pseudo-nitzschia australis (Bacillariophyceae) using rRNA-targeted probes in whole cell and sandwich hybridization formats. Phycologia 35:190–197, https://doi.org/10.2216/i0031-8884-35-3-190.1.

Scholin, C.A., G.J. Doucette, and A.D. Cembella. 2008. Prospects for developing automated systems for in situ detection of harmful algae and their toxins. Pp. 413–462 in Real-Time Coastal Observing Systems for Ecosystem Dynamics and Harmful Algal Blooms. M. Babin, C.S. Roesler, and J.J. Cullen, eds, UNESCO Publishing, Paris, France.

Scholin, C., G. Doucette, S. Jensen, B. Roman, D. Pargett, R. Marin III, C. Preston, W. Jones, J. Feldman, C. Everlove, and others. 2009. Remote detection of marine microbes, small invertebrates, harmful algae, and biotoxins using the Environmental Sample Processor (ESP). Oceanography 22(2):158–167, https://doi.org/​10.5670/oceanog.2009.46.

Scholin, C.A., R. Marin III, P.E. Miller, G.J. Doucette, C.L. Powell, P. Haydock, J. Howard, and J. Ray. 1999. DNA probes and a receptor-​binding assay for detection of Pseudo-nitzschia (Bacillariophyceae) species and domoic acid activity in cultured and natural samples. Journal of Phycology 35:1,356–1,367, https://doi.org/​10.1046/j.1529-8817.1999.3561356.x.

Scholin, C.A., E.I. Massion, D.K. Wright, D.E. Cline, E. Mellinger, and M. Brown. 2001. Aquatic autosampler device. US Patent No. 6187530.

Scholin, C.A., M.C. Villac, K.R. Buck, J.M. Krupp, D.A. Powers, G.A. Fryxell, and F.P. Chavez. 1994. Ribosomal DNA sequences discriminate among toxic and non-toxic Pseudonitzschia species. Natural Toxins 2:152–165, https://doi.org/10.1002/nt.2620020403.

Scholin, C.A., E. Vrieling, L. Peperzak, L. Rhodes, P. and Rublee. 2003. Detection of HAB species using lectin, antibody and DNA probes. Pp. 131–164 in Manual on Harmful Marine Microalgae, 2nd ed., vol. 11. G.M. Hallegraeff, D.M. Anderson, and A.D. Cembella, eds, Intergovernmental Oceanographic Commission, UNESCO, Paris, France.

Seegers, B.N., J.M. Birch, R. Marin III, C.A. Scholin, D.A. Caron, E.L. Seubert, M.D.A. Howard, G.L. Robertson, and B.H. Jones. 2015. Subsurface seeding of surface harmful algal blooms observed through the integration of autonomous gliders, moored Environmental Sample Processors, and satellite remote sensing in Southern California. Limnology and Oceanography 60:754–764, https://doi.org/​10.1002/lno.10082.

Tyrrell, J.V., P.R. Berguist, P.L. Berguist, and C.A. Scholin. 2001. Detection and enumeration of Heterosigma akashiwo and Fibrocapsa japonica (Raphidophyceae) using rRNA-targeted oligonucleotide probes. Phycologia 40:457–467, https://doi.org/​10.2216/​i0031-8884-40-5-457.1.

Ussler, W. III, P. Tavormina, C. Preston, R. Marin III, D. Pargett, S. Jensen, B. Roman, S. Shah, P.R. Girguis, J.M. Birch, and others. 2013. Autonomous in situ quantitative PCR amplification of aerobic methanotroph genes in the deep sea. Environmental Science and Technology 47:9,339−9,346, https://doi.org/10.1021/es4023199.

Varaljay, V.A., J. Robidart, C.M. Preston, S.M. Gifford, B.P. Durham, A.S. Burns, J.P. Ryan, R. Marin III, R.P. Kiene, J.P. Zehr, and others. 2015. Single-taxon field measurements of bacterial gene regulation controlling DMSP fate. The ISME Journal 9:1,677–1,686, https://doi.org/10.1038/ismej.2015.94.

Van Ness, J., and L. Chen. 1991. The use of oligonucleotide probes in chaotrope-based hybridization solutions. Nucleic Acids Research 19:5,143–5,151.

Van Ness, J., S. Kalbfleisch, C.R. Petrie, M.W. Reed, J.C. Tabone, and N.M. Vermeulen. 1991. A versatile solid support system for oligonucleotide probe-based hybridizations. Nucleic Acids Research 19:3,345–3,350.

Yamahara, K.M., E. Demir-Hilton, C.M. Preston, R. Marin III, D. Pargett, B. Roman, S. Jensen, J.M. Birch, A.B. Boehm, and C.A. Scholin. 2015. Simultaneous monitoring of faecal indicators and harmful algae using an in situ autonomous sensor. Letters in Applied Microbiology 61:130–138, https://doi.org/10.1111/lam.12432.

Copyright & Usage

This is an open access article made available under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution, and reproduction in any medium or format as long as users cite the materials appropriately, provide a link to the Creative Commons license, and indicate the changes that were made to the original content. Images, animations, videos, or other third-party material used in articles are included in the Creative Commons license unless indicated otherwise in a credit line to the material. If the material is not included in the article’s Creative Commons license, users will need to obtain permission directly from the license holder to reproduce the material.