seeing microbes from space - usc dana and david dornsife

Seeing Microbes from SpaceRemote sensing is now a critical resource for tracking marine microbialecosystem dynamics and their impact on global biogeochemical cycles

Douglas G. Capone and Ajit Subramaniam

Microbiologists studying aquaticenvironments are benefitingfrom their use of remote sensingtechnologies. With access to datagathered by remote sensors on

aircraft and satellites, microbiologists now cananalyze microbial population dynamics withgreater breadth and a novel perspective.

Remote sensing instruments exploit electro-magnetic radiation to study surface processes onearth. Passive sensors use reflected sunlight orheat being emitted by objects along the earth’ssurface, while active sensors transmit laser ormicrowaves that are then reflected back to andrecorded by the sensor. Many orbiting satellitescurrently map ocean properties such as color,surface temperature, height, wind velocities,roughness of the ocean surface, and waveheight. Plans call for additional sensors for map-ping salinity, as well as the vegetation canopyusing active light detection and ranging (LI-DAR). Although most remote sensing instru-ments are limited to near-surface properties,subsurface processes often can be inferred.

There are several advantages to using remotesensing techniques, such as accessing otherwisedifficult locations and rapidly mapping largeswaths of the earth’s surface. For example, sen-sors that are aboard polar-orbiting satellites canmap the entire surface of the earth each day.Each two-minute scene recorded by such a sat-ellite sensor, which has a 1-km spatial resolu-tion, would take 11 years to sample for a shiptraveling at about 20 km per hour.

Mapping the Oceans Using Ocean Color

One form of remote sensing uses the color ofwater to infer what it contains. For example,many of us consider the deep blue color of

oceans or other large bodies of water to meanthat they are clean, whereas the brown color ofrivers and streams mean they are carrying sus-pended mud or other materials.

This instinctive knowledge forms the basis ofocean color science. Sunlight that enters theocean can either be absorbed or scattered back(Fig. 1). Pure water absorbs most red light butstrongly scatters most blue light. Thus, openocean waters with very little material in themappear deep blue, while waters carrying dis-solved organic materials that absorb blue lightstrongly appear brown. Chlorophyll-containingmicroalgal assemblages—phytoplankton—ab-sorb both blue and red light, making phyto-plankton-containing waters look green. In addi-tion, chlorophyll emits a small fraction of theabsorbed light at a longer wavelength as redfluorescence, providing another signal for re-mote sensing. Scientists use these variations inthe color of water to estimate the amount ofphytoplankton, suspended sediment, and dis-solved organic material.

Several satellite-borne sensors, includingthe Sea-Viewing Wide Field-of-View Sensor(SeaWiFS), Moderate-Resolution Imaging Spec-troradiometer (MODIS-Terra, MODIS Aqua),Medium Resolution Imaging Spectrometer(MERIS), and the Ocean Colour Monitor (OCM),measure specific wavelengths of light emanatingfrom ocean surfaces (see the online article for a fulllist of satellite sensors). Perhaps the best and mostobvious example of the microbiological exploita-tion of satellite technology is the broad-scale map-ping of phytoplankton in the oceans (Fig. 2)(http://oceancolor.gsfc.nasa.gov). This technol-ogy enables us to describe spatial, seasonal, andinterannual patterns and dynamics of oceanicplants and is used to infer rates of photosyn-thetic carbon uptake, often referred to as pri-

Douglas G. Caponeis the Wrigley Pro-fessor of BiologicalSciences in theWrigley Institute forEnvironmentalStudies and Depart-ment of BiologicalSciences, Univer-sity of SouthernCalifornia, LosAngeles, and AjitSubramaniam is aDoherty AssociateResearch Scientistat the LamontDoherty Earth Ob-servatory of Colum-bia University, NewYork.

Volume 71, Number 4, 2005 / ASM News Y 179

mary production. Through such analyses, wemore fully understand the role of ocean micro-biota in the global carbon cycle.

Satellite Observations Provide a Means

for Detecting Specific Organisms

Interest in learning how to more fully character-ize phytoplankton populations in the great ex-panses of the world’s oceans continues to grow.We now recognize a range of “functional groups”of marine autotrophs that are characterized bytheir biogeochemical role in different elementalcycles. Scientists now can identify and quantifymonospecific blooms of certain microalgae andcyanobacteria. And, by coupling these measure-ments with ecosystem modeling, we can esti-mate the broad-scale biogeochemical impacts ofthese populations.

In many areas, including the oceans aroundAntarctica, along the eastern boundaries of theAtlantic and Pacific Oceans, and along the equa-tor (Fig. 2), a phenomenon referred to as up-welling brings nutrient-rich waters from deep inthe ocean to the surface. This phenomenon is

being studied by a suite of sensors, in-cluding those that map sea surface tem-peratures (SST), surface wind velocities,and sea surface height (SSH). These nu-trient enrichments result in high densi-ties of diatoms and other eukaryoticmicroalgae in surface waters. Dia-toms serve as major primary produc-ers in important food webs, contrib-uting substantially to the cycling ofsilicon in the sea and to the sinking ofcarbon from surface waters. Diatomsalso dominate segments of open oceanthat were experimentally fertilized(Fig. 3A). Researchers are developingalgorithms to discriminate diatomsfrom other phytoplankton.

Indeed, satellites are being used todetect a range of specific phytoplank-ters. For instance, they are used to mapthe planktonic marine cyanobacteriumTrichodesmium that occurs throughoutthe marine tropics (Fig. 4). In additionto its role in fixing carbon through pho-tosynthesis, this organism also fixes ni-trogen gas to produce organic nitrogen,

making this otherwise scarce nutrient availablein waters where it resides. Although Trichodes-mium lacks specialized heterocyst cells thatsome nitrogen-fixing cyanobacteria depend on,it contains proteinaceous vacuoles, or gas vesicles,providing cells with buoyancy and keeping suchpopulations near the surface where light is plen-tiful. Trichodesmium occurs as individualtrichomes as well as multifilament aggregates,often referred to as colonies (Fig. 4a and b).

Several optical properties make Trichodes-mium an excellent microbe for study by remotesensing. For instance, its gas vesicles are veryhighly reflective. Furthermore, unlike most eu-karyotic algae, it contains phycoerythrin as amajor accessory pigment. The absorption andfluorescence spectra of this pigment are readilydistinguished from chlorophyll a. Finally, itsnear-surface habitat (staying in a zone withinabout 50 m from the ocean surface) makes it rel-atively easy to observe. Indeed, astronauts aboardthe space shuttle frequently see and photographits more extensive blooms (Fig. 4D). Algorithmsthat are based on the six color bands detected bythe SeaWiFS satellite can be used to identifyTrichodesmium-associated chlorophyll (Fig.

F I G U R E 1

The color of the ocean is recorded by a satellite sensor by measuring the “remotesensing reflectance (Rrs)” at specific wavelengths. Rrs is the ratio of light leaving thewater (Lw) to the light incident on it (ET) and is determined by the absorption (a) andbackscattering (bb) of light in the water column (Rrs � Lw/ET � bb/(a � bb).

180 Y ASM News / Volume 71, Number 4, 2005

A Childhood at the Seashore, a Career Studying Marine Microbiology

When Douglas Capone visitedCalifornia in 1997 to interview forhis current job, the dean quizzedhim about a two-year gap duringhis undergraduate days. “I wasinvolved in some radical activitieson campus, and I was asked toleave,” Capone told the dean, whoasked in reply, “You’re not goingto do that here, are you?”

Hardly. Those indiscretionsduring the heady Vietnam Waryears of the late 1960s and early1970s marked a time of wide-spread protests and plentiful per-sonal uncertainties. Capone facedthem as an unenthusiastic premedstudent at Seton Hall Universityin South Orange, N.J. Like manyof his contemporaries, he vehe-mently opposed the war and thusparticipated along with other stu-dent activists who took over anadministration building. In 1970,Capone dropped out of school,worked at several jobs, and thenhitchhiked around the country. “Iwas drifting, trying to figure outwhere I wanted to go in my life,”he recalls.

Soon enough, Capone wasdrawn to studying the ocean, andthat is how he continues to spendhis adult life. Today he directs themarine environmental biologyprogram at the University ofSouthern California (USC) Wrig-ley Institute for EnvironmentalStudies. His research focuses onthe role and importance of marinemicrobes in major biogeochemi-cal cycles. “We study the naturalpopulations of bacteria and ar-chaea in different environmentsand try to tease out what they aredoing,” he says. “Most of my cur-

rent work is focused on the nitro-gen cycle.”

He and his colleagues are focus-ing on oceanic nitrogen fixa-tion—the biological conversion ofnitrogen gas into biologically use-ful forms of nitrogen. Capone be-lieves that nitrogen fixation maybe a key in determining how muchcarbon dioxide tropical oceanscan absorb.

After his two-year excursionfrom college, Capone enrolled atthe University of Miami, where hereceived a B.S. degree in biologyin 1973. He stayed there for hisdoctoral studies and, in 1978, re-ceived a Ph.D. in marine sciencesfrom the University of MiamiRosenstiel School of Marine andAtmospheric Science. “Havingmatured a bit, and while finishingmy basic undergraduate degree inbiology, I got into a work-studyprogram at the marine laboratoryon Virginia Key, near KeyBiscayne,” he recalls. “I was just agrunt in the laboratory, doingWinkler O2 titrations, grindingcorals and analyzing them—butthe exposure to the researchersthere and their focus on theocean’s microbial world really gotmy attention.”

Before moving to California,Capone was on the faculty at theUniversity of Maryland andserved in its center for environ-mental science in the ChesapeakeBiological Laboratory in So-lomons, Md. Earlier, he workedin the Marine Sciences ResearchCenter at the State University ofNew York at Stony Brook andwas a visiting scientist in the de-partment of chemistry at the

Brookhaven National Labora-tory, Upton, N.Y.

Capone met his wife, Linda Du-guay, a marine physiologicalecologist who is now a scienceadministrator, during graduateschool at the University of Miami.They have two daughters, 25 and20. Their older daughter works asan account manager with the Ad-visory Board Co. in Washington,D.C., while the younger is a soph-omore at USC. Both focus onbusiness, he says, adding that “theyounger one now has a minor inenvironmental sciences—possiblya concession to us.”

In a typical year, he spendsabout 30–50 days at sea. Caponefirst came to love the ocean whilegrowing up near the Jersey shore.His parents, both office workersin Newark, N.J., took Caponeand his younger sister to the shoreon weekends. By the time Caponestarted high school, they hadmoved there permanently.

“When I was young, I loved tosurf and fish, so a career that keptme close to the water seemed log-ical,” he says. “The sea has al-ways lured me. It’s been a definingfocus of my activities, both profes-sionally and recreationally. Ofcourse, marine microbiology ismore than a career—it’s a pas-sion.” When on land, he runs mostdays (often on the beach!), andenjoys skiing. But, not surpris-ingly, his favorite vacations are atthe shoreline. “A busman’s holi-day,” he says.

Marlene Cimons

Marlene Cimons is a freelance writerin Bethesda, Md.


F I G U R E 2 - 4

Fig. 2. Global annual average plant biomass map derived from the SeaWiFS satellite. The oceanic biomass is mapped as chlorophyllconcentration while the terrestrial biomass is indicated as the normalized difference vegetation index.

Fig. 3. A bloom of diatoms induced by open ocean iron fertilization experiment (SOIREE) in the Southern Ocean in February 1999 as detectedby the SeaWiFS satellite on 23 March 1999; (B) a SeaWiFS “true color” image showing blooms of Coccolithophores in the North Sea anda diazotrophic cyanobacterium, Nodularia, in the Baltic Sea from July 1999; (C) a photograph of an intense “red tide” Noctiluca bloom offSouthern California.

Fig. 4. Trichodesmium trichomes (A), colonies (B) a surface bloom in the Capricorn Channel and (D) a photo from the space shuttle of NWAustralia. The highly reflective features in (A) are gas vesicles. Each filament in (A) is about 10 um in diameter. The colony in B is about 5mm by 10 mm. The bloom seen in the space shuttle photo extends over 100 km.


5B). However, the detection threshold is rela-tively high, about 0.8 mg per cubic meter, whichrepresents a substantial bloom.

Trichodesmium is not the only microorgan-ism that is specifically detectable from space.Coccolithophores, a group of the Prymnesio-phyte algae, form calcium carbonate plates, orcoccoliths, on their outer surfaces. They partic-ipate in carbon cycling by producing both or-ganic carbon and particulate inorganic carbonfrom dissolved inorganic carbon. Coccolithplates are highly reflective at short wavelengthsand turn the water milky blue when found inhigh concentrations (Fig. 3B).

Growth of the nitrogen-fixing cyanobacte-rium Nodularia is responsible for the massivebloom visible seasonally at the center of theBaltic Sea (Fig. 3B). These cyanobacteria haveoptical properties similar to Trichodesmium,proliferate in the late summer, and have beenmapped using ocean color satellite sensors.Such cyanobacterial blooms accumulate at thesurface, changing the reflectance of microwavestransmitted by synthetic aperture radar (SAR)satellite sensors. These SAR sensors allow us tomap these blooms even in cloudy conditions andat spatial resolutions as fine as 10 m.

Other monospecific blooms can also be ob-served from space. Phaeocystis spp., anotherPrymnesiophyte, often form mucilaginous matswhen cells bloom at high latitudes such as inwaters surrounding Antarctica. The mucilagi-

nous coating gives such mats a high reflectancein the green part of the spectrum, allowing sci-entists to develop algorithms that can distin-guish Phaeocystis blooms from other phyto-plankton blooms such as those of diatoms thatalso have high reflectances. Phaeocystis and di-atoms play different roles in the carbon cycle athigh latitudes, with the latter helping to drawdown carbon when the bloom sinks. Phaeocys-tis is also biogeochemically important because itproduces dimethylsulfoniopropionate, which isdegraded to dimethyl sulfide that escapes intothe atmosphere to join the atmospheric sulfurcycle and contributes to cloud formation.

In coastal areas, noxious or toxic blooms arerecurrent and can interfere with recreationaland commercial uses of these waters. Often re-ferred to as harmful algal blooms (HABs)(http://www.whoi.edu/redtide/), they are anemergent problem. Although there are no cur-rent optically based, organism-specific algo-rithms for mapping these blooms, they often aremonospecific and can be spectacular in intensity(Fig. 3C), making them easy to detect by satel-lite. Coastal management agencies typically usesatellite images to identify locations with sub-stantial biomass to direct sampling to determinewhether they are due to HABs. Scientists at theNational Oceanic and Atmospheric Administra-tions Coastal Services Center are using remotesensing, in-situ field measurements, and buoydata to provide a HAB bulletin for the Gulf of

F I G U R E 5

True-color image of a Trichodesmium bloom (A), the Trichodesmium derived chlorophyll (B), and modeled N2 fixation (C). From Subramaniamet al., 2002, and Hood et al., 2002, reprinted with permission of Elsevier.


Mexico coastal management community (http://www.csc.noaa.gov/crs/habf/).

Beyond Chlorophyll to Other Products

and Indirect Approaches

Ocean color analysis is used to measure param-eters other than phytoplankton biomass. Forinstance, satellite imagery of global cloud coveris used to estimate the photosyntheticallyavailable radiation (PAR) available at the seasurface every day. Apart from being key tophotosynthesis, a measure of the penetration oflight in the water column is also an importantwater quality measure and K490, the diffuseattenuation coefficient at 490 nm, is a standardglobal ocean color product.

Other algorithms are used or are being devel-oped to estimate particulate inorganic carbon inthe form of liths from coccolithophores, totalsuspended solids, particulate organic carbon,and the absorption due to colored dissolvedorganic matter (CDOM) from highly refractory,riverborne organic material. Maps of CDOMhelp us to understand the influence of terrestri-ally derived organic material on the marine eco-system as well as the dynamics of dissolvedorganic matter in the open ocean. Dissolvedorganic carbon is the primary substrate for het-erotrophic marine bacterioplankton, and photo-bleaching CDOM conditions it for consumptionby bacteria. Thus, tracking CDOM may be use-ful for understanding bacterial activity in sur-face ocean waters.

Apart from ocean color, there are other satel-lite resources which may be exploited for study-ing the distribution and activity of oceanic mi-crobes. For example, although Vibrio choleraecannot be detected directly by satellite sensors,marine plankton are a significant marine reser-voir of these bacteria. In the Bay of Bengal, theannual cycle of SST is similar to that of choleracases, and SSH is a good indicator of incursionsof plankton-laden waters. Combined, the twoprovide a statistically significant correspon-dence with the incidence of cholera in Bang-ladesh.

SAR measures the roughness of the sea sur-face that can be altered by surfactants or phyto-plankton blooms at the surface. SAR, which isan active remote sensing technique, can be usedeven when clouds are present and with resolu-tions of 10 m. SAR imagery is being used, for

example, to study toxic cyanobacterial bloomsin the Baltic Sea and to map oil spills. Poten-tially, it could also be used to follow the disper-sion and microbiological degradation of suchspills.

Modeling and Scaling

One objective in remotely detecting populationsof microalgae, specific phytoplankters, or func-tional groups is to analyze their dynamics as acontext for estimating their ecological and bio-geochemical importance.

For instance, we can use remote sensing to mea-sure phytoplankton concentrations, then modelprimary production by the phytoplankton glo-bally. The growth rate of phytoplankton dependsmainly on phytoplankton concentration, theamount of light the phytoplankton receives forphotosynthesis, and factors such as temperatureand the supply of nutrients to sustain growth.Since most nutrients in the open ocean comefrom the deep where it is very cold, maps of seasurface temperatures can be used as a proxy forsurface nutrient maps. By combining satellite-based maps of incident light, phytoplanktonconcentrations, and SST, we can create globalmaps of primary production and carbon fixa-tion rates. Similarly, for a diazotroph such asTrichodesmium, we have developed models topredict in situ nitrogen fixation based on re-motely sensed biomass and solar flux (Fig. 5C).

However, although Trichodesmium can bedirectly detected only at high surface densities,these organisms are found throughout most oli-gotrophic oceanic warm waters in appreciableabundance. Indeed, warm surface waters (Fig.6A) that tend to be depleted of combined inor-ganic nitrogen such as nitrate (Fig. 6B) are hab-itats where one typically finds Trichodesmiumand other diazotrophs. Thus, we use SST mea-surements from the satellite sensors to estimatethe area of warm waters (e.g., 25°C) as a proxyfor estimating nutrient-depleted zones, thenscale these estimates based on rates of nitrogenfixation determined on oceanographic cruises.

SSH is another useful parameter with ecolog-ical relevance. SSH indicates the depth of thethermocline, the thermal discontinuity betweenwarm surface waters and cold, nutrient-richdeep waters. Through much of the oceans, SSHinversely correlates with chlorophyll concentra-tions. That is, normally, a low SSH and shallow


thermocline indicates a proximalsource of deep nutrients resulting inhigh chlorophyll. However, in certainareas of the oligotrophic ocean, such asthe southwest North Atlantic Ocean,high SSH is coincident with high chloro-phyll. This unusual finding appears toindicate an area of the ocean wherehigher levels of nitrogen fixation maysupport higher algal biomass despite apaucity of nutrients.

Remote sensing can also provide in-sights on large-scale controls of micro-biological processes in the ocean.Throughout much of the surface ocean,dissolved iron is available only in traceconcentrations (less than nanomolar).A primary source of iron is throughdeposits of atmospheric dust. Nitrogen-fixing microorganisms, particularlythose that also carry out photosynthe-sis, need relatively high quantities ofiron to satisfy the demands of special-ized enzymes. Satellite sensors havebeen used to estimate the atmosphericaerosol optical thickness, a measure ofthe particulate burden in the atmo-sphere, globally (Fig. 6C). The mostintense deposits of dust, and hence iron,into the oceans occur in the tropical North At-lantic from the Sahel desert of Africa (Fig. 6D).

Bright Prospects amid Looming

Uncertainties

Paralleling development of remote sensors is thedeployment of passive and active sensors onbuoys to monitor microbial populations andother characteristics, including nutrient concen-trations, pigment spectra, and photosyntheticrates (e.g., by fast-repetition-rate fluorometry).Perhaps the most exciting prospect from a mi-crobiological standpoint would be to link re-mote sensing with other key technology devel-opments affecting marine molecular ecology.For example, soon instruments will be deployedon buoys capable of detecting specific organ-isms, genes, their expression, and metabolic path-ways. Then, linking “sea truth” data from suchsites with information being gathered by satel-lites will greatly enhance the value of the infor-

mation being gleaned from each separate ap-proach.

The ocean optics field is moving toward de-ploying more sophisticated sensors that willlikely improve our ability to resolve and quan-tify ocean microbes and processes associatedwith their activity. For instance, the goals ofthe Earth System Science Pathfinder program,which is sponsored by the National Aeronauticsand Space Agency (NASA), include an expliciteffort to better understand phytoplankton phys-iology and study functional microbial groupsfrom space.

The proposed NASA Physiology LIDAR-Multispectral (PhyLM) mission would charac-terize key upper-ocean carbon cycle compo-nents, including phytoplankton carbon biomassand physiology. This mission would use a mul-tispectral sensor capable of measuring up to 40wavebands in the ultraviolet, visible, and nearinfrared. This instrument thus could measurephytoplankton fluorescence for a biomass indexin regions that are too optically complex forinversion algorithms. This mission would also

F I G U R E 6

Distributions of SST (A) concentrations of nitrate (B) and aerosol optical thickness (AOT)(C) in the global ocean. (D) A true color SeaWiFS image of a major dust storm offnorthwest Africa. SST and AOD are derived from the NOAA AVHRR satellite, nitrate fromthe World Ocean Atlas/ WOCE data set.


be expected to determine particle scatteringfrom which phytoplankton carbon, particleabundance, and particle size spectra can be esti-mated. Elsewhere, there is an increasing focuson remote sensing of the coastal ocean, withplans to use geostationary satellites and hyper-spectral sensors. A geostationary satellite can scanthe coast of the United States several times a day,allowing us to understand tidal effects and trans-port and diurnal changes, and would enable us toreduce interference from coastal convectiveclouds.

The upper troposphere and lower strato-sphere are regions of study for instruments onNASA’s Aura satellite, one of a triptych ofEarth-observing missions. Those instrumentsmeasure materials affecting air quality, includ-ing carbon monoxide, nitrogen dioxide, sulfurdioxide, ozone, and aerosol particulates, pro-viding global maps that can help to distinguish

between their industrial and natural sources.Aura also measures vertical distributions ofgreenhouse gases such as methane, water vapor,and ozone that will provide insights about theirproduction by microbial and physical processesin tropical upwelling regions. The Orbiting Car-bon Observatory, a satellite mission planned forlaunch in 2007, will measure carbon dioxide,another greenhouse gas that is affected by mi-crobial and human activity.

Although NASA has future plans for oceancolor sensors aboard satellites, there are no bud-geted science follow-on ocean color missions tothe Earth Observing System. This lapse may bedue, in part, to scientists not effectively explain-ing their needs for future missions. Because re-mote sensing is now a critical resource for track-ing ecosystem dynamics, any lapses in keysatellite assets will greatly constrain our abilityto detect and document these changes.

ACKNOWLEDGMENTS

We thank Ed Carpenter for discussions over the years and Claire Mahaffey for her thoughtful comments on the manuscript.Norman Kuring of NASA Goddard Space Flight Center produced the beautiful satellite images (Fig. 2A, 3B, and 5A). Thephotographs in Fig. 3C, 4A, and 4B are from Peter Franks (Scripps Institution of Oceanography), Kaori Ohki (FukuiPrefectural University), and Hans Paerl (University of North Carolina), respectively, with permission. We thank the SeaWiFSProject (Code 970.2) and the Goddard Earth Sciences Data and Information Services Center/Distributed Active Archive Center(Code 902) at the Goddard Space Flight Center, Greenbelt, MD 20771, for the production and distribution of the SeaWiFSdata. We also acknowledge the Ocean Sciences division of NSF and the Ocean Biology and Biogeochemistry Program at NASAfor sustained financial support. This is LDEO contribution number 6748.

SUGGESTED READING

Behrenfeld, M. J., E. Boss, D. A. Siegel, and D. M. Shea. 2005. Carbon-based ocean productivity and phytoplanktonphysiology from space. Global Biogeochem. Cycles 19:GB100610.1029/2004GB002299.Boyd, P., et al. 2000. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature407:695–702.Capone, D. G. 2001. Marine nitrogen fixation: what’s the fuss? Curr. Opin. Microbiol. 4:341–348.Coles, V. J., C. Wilson, and R. R. Hood. 2004. Remote sensing of new production fuelled by nitrogen fixation. Geophys. Res.Lett. 31:10.1029/2003GL019018.Hood, R., S. Subramaniam, L. May, E. Carpenter, and D. Capone. 2002. Remote estimation of nitrogen fixation byTrichodesmium. Deep-Sea Res. Part II 49(1–3):123–147.Iglesias-Rodriguez, D. M., C. W. Brown, S. C. Doney, J. Kleypas, D. Kolber, Z. Kolber, P. K. Hayes, and P. G. Falkowski.2002. Representing key phytoplankton functional groups in ocean carbon cycle models: Coccolithophorids. Global Biogeo-chemical Cycles 16(4):1100.Lobitz, B., L. Beck, A. Huq, B. Wood, G. Fuchs, A. S. G. Faruque, and R. Colwell. 2000. Climate and infectious disease: Useof remote sensing for detection of Vibrio cholerae by indirect measurement. Proc. Natl. Acad. Sci. USA 97:1438–1443.Moran, M. A., W. M. Sheldon, Jr., and R. G. Zepp. 2000. Carbon loss and optical property changes during long-termphotochemical and biological degradation of estuarine dissolved organic matter. Limnol. Oceanogr. 45:1254–1264.Sathyendranath, S., L. Watts, E. Devred, T. Platt, C. Caverhill, and H. Maass. 2004. Discrimination of diatoms from otherphytoplankton using ocean-colour data. Marine Ecol. Progress Ser. 272:59–68.Subramaniam, A., C. W. Brown, R. R. Hood, E. J. Carpenter, and D. G. Capone. 2002. Detecting Trichodesmium blooms inSeaWiFS imagery. Deep Sea Res. Part II 49 (1-3):107–121.Subramaniam, A., S. Kratzer, E. J. Carpenter and E. Soderback. 2000. Remote sensing and optical in-water measurements ofa cyanobacteria bloom in the Baltic Sea. Sixth International Conference on Remote Sensing for Marine and CoastalEnvironments, Charleston, SC, Veridian ERIM International.


seeing microbes from space - usc dana and david dornsife

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