Microbial Ecology

, Volume 67, Issue 3, pp 489–500 | Cite as

Viewing Marine Bacteria, Their Activity and Response to Environmental Drivers from Orbit

Satellite Remote Sensing of Bacteria
  • D. Jay Grimes
  • Tim E. Ford
  • Rita R. Colwell
  • Craig Baker-Austin
  • Jaime Martinez-Urtaza
  • Ajit Subramaniam
  • Douglas G. Capone
Review

Abstract

Satellite-based remote sensing of marine microorganisms has become a useful tool in predicting human health risks associated with these microscopic targets. Early applications were focused on harmful algal blooms, but more recently methods have been developed to interrogate the ocean for bacteria. As satellite-based sensors have become more sophisticated and our ability to interpret information derived from these sensors has advanced, we have progressed from merely making fascinating pictures from space to developing process models with predictive capability. Our understanding of the role of marine microorganisms in primary production and global elemental cycles has been vastly improved as has our ability to use the combination of remote sensing data and models to provide early warning systems for disease outbreaks. This manuscript will discuss current approaches to monitoring cyanobacteria and vibrios, their activity and response to environmental drivers, and will also suggest future directions.

References

  1. 1.
    Akanda AS, Jutla AS, Alam M, deMagny GC, Siddique A, Sack RB Huq A, Colwell RR, Islam S (2011) Hydroclimatic influences on seasonal and spatial cholera transmission cycles: implications for public health intervention in the Bengal Delta. Water Resour Res 47, doi: 10.1029/2010WR009914
  2. 2.
    Baker-Austin C, Trinanes JA, Taylor NG, Hartnell R, Siitonen A, Martinez-Urtaza J (2012) Emerging Vibrio risk at high latitudes in response to ocean warming. Nat Clim Chang 3:73–77CrossRefGoogle Scholar
  3. 3.
    Baker‐Austin C, Stockley L, Rangdale R, Martinez‐Urtaza J (2010) Environmental occurrence and clinical impact of Vibrio vulnificus and Vibrio parahaemolyticus: a European perspective. Environ Microbiol Rep 2:7–18CrossRefPubMedGoogle Scholar
  4. 4.
    Banakar V, deMagny GC, Jacobs J, Murtugudde R, Huq A, Wood RJ, Colwell RR (2011) Temporal and spatial variability in the distribution of Vibrio vulnificus in the Chesapeake Bay: a hindcast study. Ecohealth 8:456–467CrossRefPubMedGoogle Scholar
  5. 5.
    Behrenfeld MJ, Falkowski PG (1997) A consumer’s guide to phytoplankton primary productivity models. Limnol Oceanogr 42:1479–1491CrossRefGoogle Scholar
  6. 6.
    Binder BJ, Chisholm SW, Olson RJ, Frankel SL, Worden AZ (1996) Dynamics of picophytoplankton, ultraphytoplankton and bacteria in the central equatorial Pacific. Deep Sea Res II: Top Stud Oceanogr 43:907–931CrossRefGoogle Scholar
  7. 7.
    Borstad GA, Gower JFR, Carpenter EJ (1992) Development of algorithms for remote sensing of Trichodesmium blooms. In: Carpenter EJ, Capone DG, Rueter JG (eds) Marine pelagic cyanobacteria: Trichodesmium and other diazotrophs, vol 362. Kluwer, Dordrecht, pp 193–210CrossRefGoogle Scholar
  8. 8.
    Bowler C, Karl DM, Colwell RR (2009) Microbial oceanography in a sea of opportunity. Nature 459:180–184CrossRefPubMedGoogle Scholar
  9. 9.
    Bracher A, Vountas M, Dinter T, Burrows JP, Rottgers R, Peeken I (2009) Quantitative observation of cyanobacteria and diatoms from space using PhytoDOAS on SCIAMACHY data. Biogeosciences 6:751–764CrossRefGoogle Scholar
  10. 10.
    Budd JW, Beeton AM, Stumpf RP, Culver DA, Kerfoot WC Presented at the International Association of Theoretical and Applied Limnology, StuttgartGoogle Scholar
  11. 11.
    Budd JW, Drummer TD, Nalepa TF, Fahnenstiel GL (2001) Remote sensing of biotic effects: Zebra mussels (Dreissena polymorpha) influence on water clarity in Saginaw Bay, Lake Huron. Limnol Oceanogr 46:213–223CrossRefGoogle Scholar
  12. 12.
    Capone DG, Subramaniam A, Montoya JP, Humborg C, Voss M, Pollehne F, Carpenter EJ (1998) An extensive bloom of the diazotrophic cyanobacterium, Trichodesmium, in the Central Arabian Sea during the spring intermonsoon. Mar Ecol Prog Ser 172:281–292CrossRefGoogle Scholar
  13. 13.
    Colwell RR (1996) Global climate and infectious disease: the cholera paradigm. Science 274:2025–2031CrossRefPubMedGoogle Scholar
  14. 14.
    Colwell RR, Spira WM, William BG III (1992) The ecology of Vibrio cholerae. In: Barua D (ed) Cholera. Plenum, New York, pp 107–127CrossRefGoogle Scholar
  15. 15.
    Cox PA, Banack SA, Murch SJ, Rasmussen U, Tien G, Bidigare RR, Metcalf JS, Morrison LF, Codd GA, Bergman B (2005) Diverse taxa of cyanobacteria produce beta-N-methylamino-L-alanine, a neurotoxic amino acid. Proc Natl Acad Sci U S A 102:5074–5078PubMedCentralCrossRefPubMedGoogle Scholar
  16. 16.
    deMagny GC, Mozumder PK, Grim CJ, Hasan NA, Naser MN, Alam M, Sack RB, Huq A, Colwell RR (2011) Role of zooplankton diversity in Vibrio cholerae population dynamics and in the incidence of cholera in the Bangladesh Sundarbans. Appl Environ Microbiol 77:6125–6132CrossRefGoogle Scholar
  17. 17.
    deMagny GC, Thiaw W, Kumar V, Manga NM, Diop BM, Gueye L, Kamara M, Roche B, Murtugudde R, Colwell RR (2012) Cholera outbreak in Senegal in 2005: was climate a factor? PloS ONE 7:e44577CrossRefGoogle Scholar
  18. 18.
    De Moraes Rudorff N, Kampel M (2012) Orbital remote sensing of phytoplankton functional types: a new review. Int J Remote Sens 33:1967–1990CrossRefGoogle Scholar
  19. 19.
    Demarcq H, Reygondeau G, Alvain S, Vantrepotte V (2011) Monitoring marine phytoplankton seasonality from space. Remote Sens Environ 117: 211–222Google Scholar
  20. 20.
    Devassy VP, Bhattathiri PMA, Qasim SZ (1978) Trichodesmium phenomenon. Indian J Mar Sci 7:168–186Google Scholar
  21. 21.
    Dupouy C, Neveux J, Dirberg G, Röttgers R, Barboza Tenório MM, Ouillon S (2008) Bio-optical properties of the marine cyanobacteria Trichodesmium spp. J Appl Remote Sens 2:023503CrossRefGoogle Scholar
  22. 22.
    Epstein PR, Ford TE, Colwell RR (1993) Marine ecosystems. Lancet 342:1216–1219CrossRefPubMedGoogle Scholar
  23. 23.
    Fawcett S, Ward B (2011) Phytoplankton succession and nitrogen utilization during the development of an upwelling bloom. Mar Ecol Prog Ser 428:13–31CrossRefGoogle Scholar
  24. 24.
    Ford T, Colwell R (1996) A global decline in microbiological quality of water: a call for action. Washington, DC: American Academy of MicrobiologyGoogle Scholar
  25. 25.
    Ford TE, Colwell RR, Rose JB, Morse SS, Rogers DJ, Yates TL (2009) Using satellite images of environmental changes to predict infectious disease outbreaks. Emerg Infect Dis 15:1341PubMedCentralCrossRefPubMedGoogle Scholar
  26. 26.
    Frischer M, Danforth J, Foy T, Juraske R (2005) Bioluminescent bacteria as indicators of chemical contamination of coastal waters. J Environ Qual 34:1328–1336CrossRefPubMedGoogle Scholar
  27. 27.
    Garver SA, Siegel DA (1994) Variability in near-surface particulate absorption spectra: what can a satellite ocean color imager see? Limnol Oceanogr 39:1349–1367CrossRefGoogle Scholar
  28. 28.
    Haddock SH, Moline MA, Case JF (2010) Bioluminescence in the sea. Ann Rev Mar Sci 2:443–493CrossRefPubMedGoogle Scholar
  29. 29.
    Hawser SP, Codd GA, Carpenter EJ, Capone DG (1991) A neurotoxic factor associated with the bloom-forming cyanobacterium Trichodesmium. Toxicon 29:277–278CrossRefPubMedGoogle Scholar
  30. 30.
    Hu CM, Cannizzaro J, Carder KL, Muller-Karger FE, Hardy R (2010) Remote detection of Trichodesmium blooms in optically complex coastal waters: examples with MODIS full-spectral data. Remote Sens Environ 114:2048–2058CrossRefGoogle Scholar
  31. 31.
    Huq A, West P, Small E, Huq M, Colwell R (1984) Influence of water temperature, salinity, and pH on survival and growth of toxigenic Vibrio cholerae serovar 01 associated with live copepods in laboratory microcosms. Appl Environ Microbiol 48:420–424PubMedCentralPubMedGoogle Scholar
  32. 32.
    Johnson CN, Flowers AR, Noriea N, Zimmerman A, Bowers J, DePaola A, Grimes DJ (2010) Relationships between environmental factors and pathogenic Vibrios in the Northern Gulf of Mexico. Appl Environ Microbiol 76:7076–7084PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Johnson CN, Bowers JC, Griffitt KJ, Molina V, Clostio RW, Pei S, Laws E, Paranjpye RN, Strom MS, Chen A, Hasan NA, Huq A, Noriea III NF, Grimes DJ, Colwel RR (2012) Ecology of Vibrio parahaemolyticus and Vibrio vulnificus in the coastal and estuarine waters of Louisiana, Maryland, Mississippi, and Washington (United States). Appl Environ Microbiol 78:7249–7257Google Scholar
  34. 34.
    Jutla AS, Akanda AS, Griffiths JK, Colwell R, Islam S (2011) Warming oceans, phytoplankton, and river discharge: implications for cholera outbreaks. Am J Trop Med Hyg 85:303PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Jutla AS, Akanda AS, Islam S (2010) Tracking cholera in coastal regions using satellite observations1. JAWRA J Am Water Resour Assoc 46:651–662CrossRefPubMedGoogle Scholar
  36. 36.
    Kahru M, Leppanen J-M, Rud O (1993) Cyanobacterial blooms cause heating of the sea surface. Mar Ecol Prog Ser 191:1–7CrossRefGoogle Scholar
  37. 37.
    Kahru M, Leppanen JM, Rud O, Savchuk OP (2000) Cyanobacteria blooms in the Gulf of Finland triggered by saltwater inflow into the Baltic Sea. Mar Ecol Prog Ser 207:13–18CrossRefGoogle Scholar
  38. 38.
    Kuchler DA, Jupp DLB (1988) Shuttle photograph captures massive phytoplankton bloom in the Great Barrier Reef. Int J Remote Sens 9:1299–1301CrossRefGoogle Scholar
  39. 39.
    Kutser T (2009) Passive optical remote sensing of cyanobacteria and other intense phytoplankton blooms in coastal and inland waters. Int J Remote Sens 30:4401–4425CrossRefGoogle Scholar
  40. 40.
    Lapota D, Galt C, Losee JR, Huddell HD, Orzech JK, Nealson KH (1988) Observations and measurements of planktonic bioluminescence in and around a milky sea. J Exp Mar Biol Ecol 119:55–81CrossRefGoogle Scholar
  41. 41.
    Lenes JM, Heil CA (2010) A historical analysis of the potential nutrient supply from the N2 fixing marine cyanobacterium Trichodesmium spp. to Karenia brevis blooms in the eastern Gulf of Mexico. J Plankton Res 32:1421–1431CrossRefGoogle Scholar
  42. 42.
    Lima FP, Wethey DS (2012) Three decades of high-resolution coastal sea surface temperatures reveal more than warming. Nat commun. doi: 10.1038/ncomms1713Google Scholar
  43. 43.
    Lobitz B, Beck L, Huq A, Wood B, Fuchs G, Faruque ASG, Colwell R (2000) Climate and infectious disease: use of remote sensing for detection of Vibrio cholerae by indirect measurement. Proc Natl Acad Sci U S A 97:1438–1443PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Martinez-Urtaza J, Huapava B, Gavilan RG, Blanco-Abad V, Ansede-Bermejo J, Cadarso-Suarez C, Figueiras A, Trinanes J (2008) Emergence of Asiatic vibrio diseases in South America in phase with El Niño. Epidemiology 19:829–837CrossRefPubMedGoogle Scholar
  45. 45.
    Martinez-Urtaza J, Blanco-Abad V, Rodriguez-Castro A, Ansede-Bermejo J, Miranda A, Rodriguez-Alvarez MX (2011) Ecological determinants of the occurrence and dynamics of Vibrio parahaemolyticus in offshore areas. ISME J 6:994–1006PubMedCentralCrossRefPubMedGoogle Scholar
  46. 46.
    Martinez-Urtaza J, Bowers JC, Trinanes J, DePaola A (2010) Climate anomalies and the increasing risk of Vibrio parahaemolyticus and Vibrio vulnificus illnesses. Food Res Int 43:1780–1790CrossRefGoogle Scholar
  47. 47.
    McKinna LIW, Furnas MJ, Ridd PV (2011) A simple, binary classification algorithm for the detection of Trichodesmium spp. within the Great Barrier Reef using MODIS imagery. Limnol Oceanogr: Methods 9:50–66Google Scholar
  48. 48.
    Mendelsohn J, Dawson T (2008) Climate and cholera in KwaZulu-Natal, South Africa: the role of environmental factors and implications for epidemic preparedness. Int J Hyg Environ Health 211:156–162CrossRefPubMedGoogle Scholar
  49. 49.
    Metsamaa L, Kutser T, Strombeck N (2006) Recognising cyanobacterial blooms based on their optical signature: a modelling study. Boreal Environ Res 11:493–506Google Scholar
  50. 50.
    Miller SD, Haddock SHD, Elvidge CD, Lee TF (2005) Detection of a bioluminescent milky sea from space. Proc Natl Acad Sci U S A 102:14181–14184PubMedCentralCrossRefPubMedGoogle Scholar
  51. 51.
    Morel A (1997) Consequences of a Synechococcus bloom upon the optical properties of oceanic (case 1) waters. Limnol Oceanogr 42:1746–1754CrossRefGoogle Scholar
  52. 52.
    Nair A, Sathyendranath S, Platt T, Morales J, Stuart V, Forget MH, Devred E, Bouman H (2008) Remote sensing of phytoplankton functional types. Remote Sens Environ 112:3366–3375CrossRefGoogle Scholar
  53. 53.
    Najjar RG, Pyke CR, Adams MB, Breitburg D, Hershner C, Kemp M, Howarth R, Mulholland MR, Paolisso M, Secor D (2010) Potential climate-change impacts on the Chesapeake Bay. Estuar Coast Shelf Sci 86:1–20CrossRefGoogle Scholar
  54. 54.
    Nealson KH, Hastings J (2006) Quorum sensing on a global scale: massive numbers of bioluminescent bacteria make milky seas. Appl Environ Microbiol 72:2295–2297PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Olson RJ, Chisholm SW, Zettler ER, Altabet MA, Dusenberry JA (1990) Spatial and temporal distributions of prochlorophyte picoplankton in the North Atlantic Ocean. Deep Sea Research Part A. Oceanogr Res Pap 37:1033–1051CrossRefGoogle Scholar
  56. 56.
    Phillips A, DePaola A, Bowers J, Ladner S, Grimes DJ (2007) An evaluation of the use of remotely sensed parameters for prediction of incidence and risk associated with Vibrio parahaemolyticus in Gulf Coast oysters (Crassostrea virginica). J Food Prot 70:879–888PubMedGoogle Scholar
  57. 57.
    Reyburn R, Kim DR, Emch M, Khatib A, von Seidlein L, Ali M (2011) Climate variability and the outbreaks of cholera in Zanzibar, East Africa: a time series analysis. Am J Trop Med Hyg 84:862PubMedCentralCrossRefPubMedGoogle Scholar
  58. 58.
    Rörig LR, Yunes JS, Kuroshima KN, Schetinni CAF, Pezzuto PR, Proença L (1998) Studies on the ecology and toxicity of Trichodesmium spp. blooms in southern Brazilian coastal waters. Harmful Algae 1:22–25Google Scholar
  59. 59.
    Samadi A, Chowdhury N, Huq M, Khan M (1983) Seasonality of classical and El Tor cholera in Dhaka, Bangladesh: 17 year trends. Trans R Soc Trop Med Hyg 77:853CrossRefPubMedGoogle Scholar
  60. 60.
    Shapiro R, Altekruse S, Hutwagner L, Bishop R, Hammond R, Wilson S, Ray B, Thompson S, Tauxe R, Griffin P (1998) The role of Gulf Coast oysters harvested in warmer months in Vibrio vulnificus infections in the United States, 1988–1996. J Infect Dis 178:752–759CrossRefPubMedGoogle Scholar
  61. 61.
    Simis SGH, Ruiz-Verdú A, Domínguez-Gómez JA, Peña-Martinez R, Peters SWM, Gons HJ (2007) Influence of phytoplankton pigment composition on remote sensing of cyanobacterial biomass. Remote Sens Environ 106:414–427CrossRefGoogle Scholar
  62. 62.
    Sivonen K, Kononen K, Carmichael W, Dahlem A, Rinehart K, Kiviranta J, Niemela S (1989) Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and structure of the toxin. Appl Environ Microbiol 55:1990–1995PubMedCentralPubMedGoogle Scholar
  63. 63.
    Stumpf RP, Tomlinson MC (2005) Remote sensing of harmful algal blooms. In: Miller RL, Del Castillo CE, McKee BA (eds) Remote sensing of coastal aquatic environments. Springer, Dordrecht, pp. 277–296Google Scholar
  64. 64.
    Subramaniam A, Carpenter EJ (1994) An empirically derived protocol for the detection of blooms of the marine cyanobacrerium Trichodesmium using CZCS imagery. Int J Remote Sens 15(8):1559–1569CrossRefGoogle Scholar
  65. 65.
    Subramaniam A, Carpenter EJ, Falkowski PG (1999) Bio-optical properties of the marine diazotrophic cyanobacteria Trichodesmium spp. II. A reflectance model for remote sensing. Limnol Oceanogr 44:618–627CrossRefGoogle Scholar
  66. 66.
    Subramaniam A, Hood RR, Brown CW, Carpenter EJ, Capone DG (2002) Detecting Trichodesmium blooms in SeaWiFS imagery. Deep_Sea Research, Part II, 1st Special Issue on the U.S. JGOFS Synth Model Proj 49:107–121Google Scholar
  67. 67.
    Tang DL, Di BP, Wei G, Ni IH, Oh IS, Wang SF (2006) Spatial, seasonal and species variations of harmful algal blooms in the South Yellow Sea and East China Sea. Hydrobiologia 568:245–253CrossRefGoogle Scholar
  68. 68.
    Vezzulli L, Brettar I, Pezzati E, Reid PC, Colwell RR, Höfle MG, Pruzzo C (2011) Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME J 6:21–30PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Westberry TK, Siegel DA, Subramaniam A (2005) An improved bio-optical model for the remote sensing of Trichodesmium spp. blooms. J. Geophys. Res 110:C06012, doi:10.1029/2004JC002517
  70. 70.
    WHO (2003) Guidelines for safe recreational water environments. World Health Organization, Geneva, pp. 136–158, vol. 1.Google Scholar
  71. 71.
    Wilson C (2003) Late summer chlorophyll blooms in the oligotrophic North Pacific Subtropical Gyre. Geophys Res Lett 30. OCE 4-1 to 4-4. doi:10.1029/2003GL017770
  72. 72.
    Xu H, Zhu G, Qin B, Paerl HW (2013) Growth response of Microcystis spp. to iron enrichment in different regions of Lake Taihu, China. Hydrobiologia 700:187–202CrossRefGoogle Scholar
  73. 73.
    Zhang Z, Deng Z-Q, Rusch K, Gutierrez WM, Chenier K (2010) Remote sensing algorithms for estimating enterococcus concentration in coastal Louisiana Beaches, The 5th International Conference on Environmental Science and Technology, Houston, TexasGoogle Scholar
  74. 74.
    Zimmerman A, DePaola A, Bowers J, Krantz J, Nordstrom J, Johnson CN, Grimes DJ (2007) Variability of total and pathogenic Vibrio parahaemolyticus densities in northern Gulf of Mexico water and oysters. Appl Environ Microbiol 73:7589–7596PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • D. Jay Grimes
    • 1
  • Tim E. Ford
    • 2
  • Rita R. Colwell
    • 3
  • Craig Baker-Austin
    • 4
  • Jaime Martinez-Urtaza
    • 5
  • Ajit Subramaniam
    • 6
  • Douglas G. Capone
    • 7
  1. 1.Gulf Coast Research LaboratoryThe University of Southern MississippiOcean SpringsUSA
  2. 2.University of New EnglandPortlandUSA
  3. 3.Center for Bioinformatics and Computational Biology, UMIACSUniversity of MarylandCollege ParkUSA
  4. 4.Centre for Environment, Fisheries and Aquaculture Science (Cefas)WeymouthUK
  5. 5.Department of Biology and BiochemistryUniversity of BathBathUK
  6. 6.Lamont-Doherty Earth ObservatoryColumbia UniversityPalisadesUSA
  7. 7.Wrigley Institute for Environmental StudiesUniversity of Southern CaliforniaLos AngelesUSA

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