Aerobiologia 19: 143–157, 2003.© 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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Atmospheric microbiology in the northern Caribbean during African dustevents

Dale W. Griffin1,∗, Christina A. Kellogg1, Virginia H. Garrison1, John T. Lisle1, Timothy C.Borden2 & Eugene A. Shinn1

1Center for Coastal and Watershed Studies, US Geological Survey, St. Petersburg, FL 33701, USA; 2Volunteer,Center for Coastal and Watershed Studies, US Geological Survey, St. Petersburg, FL 33701, USA(∗author for correspondence: Phone: (727) 803-8747 extension 3113; Fax: (727) 803-2031;E-mail: dgriffin@usgs.gov)

Received 13 May 2003; accepted in final form 27 May 2003

Key words: aerobiology, African dust, bacteria, Caribbean, ecosystem health, fungi, microbiology, public health

Abstract

Between July 2000 and August 2001 forty-three air samples were collected in the northern Caribbean: Twenty-sixin the US Virgin Islands, and 17 samples aboard ship during two 1-week cruises. Samples were collected duringAfrican dust events and non-dust conditions and screened for the presence of culturable bacteria and fungi. A totalof 3,652 liters of air were collected during non-dust conditions, with 19 bacteria and 28 fungi being recovered.During dust conditions a total of 2,369 liters of air were screened resulting in the recovery of 171 bacteria and 76fungi. A statistically significant difference was found between the two data sets. These results support previousAfrican dust research and further demonstrate that dust particles can serve as a vessel for the global dispersion ofbacteria and fungi. Dustborne microorganisms may play a significant role in the ecology and health of downwindecosystems.

1. Introduction

While the study of long range transport of micro-organisms in Earth’s atmosphere may appear to be anemerging field, in fact, it has a long history with arich pedigree of well-known scientists. In the early1800’s, Ehrenberg described “Infusoria” (microorga-nisms) in samples of African dust collected aboard theH.M.S. Beagle by Charles Darwin while traversing thecoast of northwestern Africa (Ehrenberg 1830; Darwin1846). In 1861, Louis Pasteur described bacteria andmolds he collected from the atmosphere while in themountains (Pasteur 1861). In a 1935 publication, FredMeier wrote (Meier 1935):

“. . . the red-winged monoplane piloted by CharlesA. Lindbergh soared away from Flushing Bay onJuly 9 1933, bound for aerial exploration near theArctic Circle, there began an unusual botanicalcollecting trip. Mrs. Lindbergh was prepared to flythe ship during intervals when her husband might

be occupied with manipulations of an instrumentnew to transatlantic airplanes . . . noncommittallycalled the ‘sky hook’, it was planned to make col-lections of microorganisms from the atmospherealong the course of flight”.

This paper described microorganisms and otherparticles which, were collected while in flight overopen Arctic and Atlantic waters and led to furtherpublished work describing a similar survey of theCaribbean atmosphere (Meier 1936). Dr. Meier wasaggressively pushing the field forward in his pursuit ofunderstanding the global dispersion of plant rusts andother pathogenic microorganisms, but unfortunatelywas lost at sea during a flight to collect air samples. Amajority of documented historical aero-microbiologyscientists have had two things in common, whilefascinated by the presence of microorganisms at vari-ous altitudes in Earth’s atmosphere, they ultimatelypursued another path in the field of microbiology.

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One of the current estimates on the quantity ofsoil or sediment (dried river and lakebeds) that movesome distance in the planet’s atmosphere each yearis approximately 2 × 109 metric tons (Perkins 2001).The single largest source of soil to Earth’s atmosphereeach year is the Saharan/Sahel region of North Africa(Moulin et al. 1997; Goudie and Middleton 2001; Per-kins 2001). This airborne African soil, which is alsoknown as African dust moves off the African coastlinealmost year round. While at times it may move intoEurope or the Middle East it generally moves off theNorthwest coast of Africa and is transported to theAmericas and Caribbean by the tropical tradewinds(Figure 1). During the North American summer (maxi-mum transport between latitudes 15◦ and 25◦ North,June through October), African dust cloud movementis generally toward the North/Central Caribbean andSoutheastern United States and in the North Americanwinter (November through May), toward the SouthCaribbean and South America (Graham and Duce1979). The dust clouds cross the Atlantic in 5–7 days,and are visible both via satellite imagery (Figure 1)and the naked eye. Figure 2 illustrates how Caribbeanair quality is impacted by the arrival of African dust.

There are both benefits and potential hazards tosoils moving through the planet’s atmosphere. Oneof the benefits of the redistribution of soils via theatmosphere is many terrestrial plants derive nutri-ents from dust-fallout in down-wind ecosystems suchas the South American (African dust) (Swap et al.1992; Swap et al. 1996) and Hawaiian rainforests(Asian desert dust from the Gobi and Takla Makandeserts) (Chadwick et al. 1999). Negative impacts ofdust movement include the transport of toxins suchas pesticide and herbicide-laden soils (O’Malley andMcCurdy 1990; Barrie et al. 1992; O’Hara et al.2000), harmful algal blooms (Walsh and Steidinger2001) and the long-range movement of pathogenicmicroorganisms (Weir et al. 2000; Griffin et al.2001a). One of our interests is the microbial eco-logy of Earth’s atmosphere, particularly as it pertainsto soil-associated microbes that are considered patho-genic to both terrestrial and aquatic life forms. In2001, we described the abundance and types of micro-organisms that were collected from a small set of airsamples taken over St. John, US Virgin Islands (USVI)during both normal and African dust-event conditions(Griffin et al. 2001a). In this paper we present datafrom samples collected in the Caribbean at varioussites on St. John and St. Thomas, USVI and while atsea aboard ship.

2. Material and methods

2.1. Sample sites

The USVI are located at the top of the Lesser AntillesIsland chain, just below Puerto Rico (approximately18◦ N, 65◦ W). The USVI’s three main islands are St.Thomas, St. John, and St. Croix. Samples sites in theUSVI included Lind Point, Mamey Peak and SabbatPoint on St. John, and Deck Point on St. Thomas.In addition, two offshore samples were also collectedwindward of each island as indicated in Table 1. RoyalCaribbean’s “Explorer of the seas” is a traditionalcruise ship that also offers laboratory space and con-tinuous atmospheric and water data collection froma variety of sensors. At the time of our cruises, theship’s cruise track circled from Miami, FL to Nassau,Bahamas, then St. Thomas, USVI followed by stopsin Puerto Rico and Haiti before returning to Miami(Figure 3). Samples taken aboard ship were collectedover a one-week period in June and July of 2001. Onthe June cruise the samples were taken outside of theatmospheric lab located on the foremost upper deckof the ship and in July from the bowsprit. Sampleswere only collected while underway and with a head-wind to limit ship-borne contamination of the samples.Sample site locations are illustrated in Figure 3. Steriletechnique was used at all times. A laminar flow hoodwas used for handling all samples with the exceptionof those taken aboard ship. Laboratory contaminationaboard ship was evaluated by exposing a plate of R2Aagar on the workbench while manipulating samplefilters.

2.2. Air samples for isolation of microbes

Presterilized filter housings containing 47 mm dia-meter, 0.2 µm pore-size filter membranes were usedto collect all air samples (Fisher Scientific, Atlanta,GA. catalog # 09-74030G.). The filter housings wereremoved from their respective sterile bags, placed onan analytical filter manifold, lids removed and vacuumapplied using a vacuum pump for a set period of time.Airflow rates through the filters ranged from 6.5 to28.4 liters minute−1 for 8 to 20 minutes per sample.To control for handling contamination, an additionalfilter housing was removed from its bag, placed onthe manifold and allowed to sit for one-minute withoutremoving the lid or turning on the vacuum. Filter hous-ings were then removed from the manifold, lids sealedwith parafilm, replaced in their respective bags, sealed

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Figure 1. SeaWiFS image, August 8, 2001. African desert dust forms an atmospheric bridge between Africa and the Caribbean. Image providedby the SeaWiFS Project, NASA/Goddard Space Flight Center and ORBIMAGE.

Figure 2. Sapphire Bay, St. Thomas, US Virgin Islands, looking down island. Top image – July 31, 2001, ∼1pm. Bottom image – August 8,2001, ∼9am. These photos show the marked decrease in visibility associated with an African dust event moving through the area.

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Table 1. Caribbean “dust” and “non-dust” samples, July 18, 2000 through August 8, 2001

Date Time Sample site Conditions Wind Wind Equivalent # of CFU2

speed direction volume of air Bacteria Fungi

(m s−1) (degrees) sampled (L) Total # # L−1 Total # # L−1

07-18-00 1200 Lind Pt., St. John, USVI No dust 2.5 64 70 7 0.100 4 0.05707-23-00 1305 Lind Pt., St. John, USVI Dust 3.9 83 88 14 0.159 5 0.05707-26-00 1000 Lind Pt., St. John, USVI Dust 3.1 119 102 36 0.353 5 0.04907-27-00 1100 Lind Pt., St. John, USVI Dust 4.2 77 74 7 0.091 2 0.02707-28-00 1300 Lind Pt., St. John, USVI Dust 4.2 103 135 28 0.207 7 0.05210-01-00 1740 Mamey Peak, St. John, USVI No dust 3.4 97 103 0 <0.0103 2 0.02010-08-00 0808 Mamey Peak, St. John, USVI No dust 3.7 125 131 0 <0.008 2 0.01511-19-00 1500 Offshore, windward, St. John, USVI No dust 5.4 66 83 0 <0.012 0 <0.01202-17-01 1230 Sabbat Pt., St. John, USVI No dust 3.0 127 99 0 <0.010 2 0.02003-03-01 1200 Sabbat Pt., St. John, USVI No dust 2.8 126 97 0 <0.010 0 <0.01003-09-01 1417 Sabbat Pt., St. John, USVI No dust 6.2 147 188 0 <0.005 2 0.01103-17-01 1130 Sabbat Pt., St. John, USVI No dust 3.6 105 195 0 <0.005 0 <0.00503-22-01 1108 Sabbat Pt., St. John, USVI No dust 6.5 154 169 0 <0.006 1 0.00604-04-01 1048 Sabbat Pt., St. John, USVI No dust 3.3 125 179 0 <0.006 0 <0.00604-15-01 1139 Sabbat Pt., St. John, USVI No dust 5.2 156 186 0 <0.005 0 <0.00504-18-01 0926 Sabbat Pt., St. John, USVI Dust/humid 7.3 147 83 0 <0.012 0 <0.01204-18-01 0942 Sabbat Pt., St. John, USVI Dust/humid 7.3 147 71 0 <0.014 0 <0.01404-18-01 0959 Sabbat Pt., St. John, USVI Dust/humid 7.3 147 120 0 <0.008 0 <0.00805-15-01 1750 Sabbat Pt., St. John, USVI Light dust 4.4 152 170 0 <0.006 1 0.00605-19-01 1016 Sabbat Pt., St. John, USVI No dust 9.3 147 168 0 <0.006 0 <0.00606-03-01 2105 Offshore, cruise (site A, Figure 3) No dust 4.5 89.7 124 2 0.020 0 <0.00806-04-01 1005 Offshore, cruise (site B, Figure 3) No dust 5.1 96.2 124 0 <0.008 0 <0.00806-04-01 2000 Offshore, cruise (site C, Figure 3) No dust 8.2 56.8 124 0 <0.008 0 <0.00806-05-01 1945 Offshore, cruise (site D, Figure 3) No dust 7.7 94.2 124 1 0.008 5 0.04006-06-01 1616 Offshore, cruise (site E, Figure 3) No dust, 13.1 76.8 124 0 <0.008 1 0.008

haze/humid06-07-01 2056 Offshore, cruise (site F, Figure 3) No dust, 11.4 78.9 124 0 <0.008 0 <0.008

haze/humid06-08-01 0930 Offshore, cruise (site G, Figure 3) No dust 5.3 98.3 124 0 <0.008 3 0.02406-08-01 1900 Offshore, cruise (site H, Figure 3) No dust, 4.8 99.9 124 8 0.066 1 0.008

haze/humid07-03-01 0918 Sabbat Pt., St. John, USVI Dust 3.4 76 169 1 0.006 1 0.00607-03-01 1222 Lind Pt., St. John, USVI Dust 4.3 64 166 1 0.006 1 0.00607-07-01 0928 Lind Pt., St. John, USVI Dust 4.2 114 199 1 0.005 0 <0.00507-22-01 2040 Offshore, cruise (site A, Figure 3) No dust 3.0 156.3 124 0 <0.008 1 0.00807-23-01 1040 Offshore, cruise (site B, Figure 3) No dust 9.4 73.4 124 0 <0.008 0 <0.00807-23-01 2107 Offshore, cruise (site C, Figure 3) No dust 6.9 102.4 124 1 0.008 3 0.02407-24-01 2105 Offshore, cruise (site D, Figure 3) No dust 10.1 82.2 124 0 <0.008 0 <0.00807-25-01 1706 Offshore, cruise (site E, Figure 3) No dust 11.8 70.6 124 0 <0.008 0 <0.00807-26-01 2041 Offshore, cruise (site F, Figure 3) No dust 12.5 70.0 124 0 <0.008 0 <0.00807-27-01 0945 Offshore, cruise (site G, Figure 3) No dust 10.9 92.9 124 0 <0.008 1 0.00807-27-01 1814 Offshore, cruise (site H, Figure 3) No dust 10.3 91.3 124 0 <0.008 0 <0.00807-30-01 Offshore, Little St. James Is., USVI Dust 5.8 ESE1 248 10 0.040 6 0.02408-08-01 0830 Deck Pt., St. Thomas, USVI Dust 3.4 ESE 248 46 0.185 22 0.09008-08-01 1105 Deck Pt., St. Thomas, USVI Dust 3.1 ESE 248 5 0.020 12 0.04808-08-01 1145 Deck Pt., St. Thomas, USVI Dust 3.1 ESE 248 22 0.090 14 0.056

ESE1 = Wind from East-southeast (ESE) as noted during sampling (no National Park Service direction data available for those dates).CFU2 = Colony forming unit. A term used to describe a colony of bacteria or fungi believed to have originated from a single cell.<#3 = Value based on a detection limit of one colony forming unit for the given equivalent volume of air sampled.Total volume of no dust samples = 3652 total liters, from which 47 bacteria/fungi CFU were recovered = 0.013CFU L−1.Total volume of dust samples = 2369 total liters, from which 247 bacteria/fungi CFU were recovered = 0.104CFU L−1.2001 Offshore cruise samples collected aboard Royal Caribbean’s “Explorer of the Seas”.

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Figure 3. Royal Caribbean’s “Explorer of the Seas” Cruise track and sample points for June and July 2001. Base map image courtesy ofLandsat.org, Global Landsat-7 Search Engine and Viewer http://foliage.geo.msu.edu/global/viewerhtm.

with tape and either transported to the ship labora-tory or for the USVI samples, refrigerated at 4 ◦Cuntil shipment to the United States Geological Survey(USGS) microbiological laboratory in St. Petersburg,Florida. R2A agar (Fisher Scientific, Atlanta, GA.Catalog # DF1826-17-1) (Reasoner and Geldreich1985), was utilized for microbial culture-based ana-lysis. The sample filters were either placed whole orcut in half using sterile scissors and one half of thefilter placed on R2A agar plates, sample side up. Theremaining half of cut filters were stored via refrigera-tion at 4 ◦C. The filters placed on R2A were incubatedin the dark at room temperature (∼23 ◦C) and moni-tored for growth over a 48-hour period (Figure 4).Fungal and bacterial colonies were isolated from eachother by isolation streaking on to fresh plates of R2A.

Once isolated, colonies were grown overnight at roomtemperature on a tabletop rocker set at low speed inTryptic Soy Broth (Fisher Scientific, Atlanta, GA.Catalog # DF0370-17-3). The following day 1 mlof each culture was transferred to a sterile cryogenicstorage tube containing 200 µl of sterile glycerol andstored at –70 ◦C.

2.3. Genetic identification of prokaryotes

The polymerase chain reaction (PCR) was used for16S rDNA amplification using a universal prokaryoteprimer set (Upstream = 5′-CCGAATTCGTCGACAACAGAGTTTGATCCTGGCTCAG-3′, Downstream =5′-CCCGGGATCCAAGCTTACGGCTACCTTGTTACGACTT-3′) (Grasby et al. 2003). For DNA

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Figure 4. Microbial growth on a sample filter collected during anAfrican dust event in the US Virgin Islands, after 96 hours of incub-ation. Sample collected from Deck Point, St. Thomas, US VirginIslands on 8 August, 2001 at 1145 am.

extraction, bacterial colonies were touched witha sterile pipette tip, and the tip was then used toinoculate 180 µl of lysis buffer recommended forextraction of DNA from gram positive bacteria ina DNeasy Tissue Kit (Qiagen Inc., Valencia, CA.Catalog # 69504). The DNeasy Tissue Kit protocolwas followed and purified DNA was eluted in 100 µlof the kit elution buffer. Five microliters of purifiedDNA were used for PCR. The PCR master mixrecipe per reaction was: 10 µl of GeneAmp 10X PCRbuffer (Promega, Madison, WI. Catalog # M1901),12 µl of 25mM MgCl2 (Promega, Madison, WI.Catalog # A3511), 2 µl of 100mM dNTP mix(Promega, Madison, WI. Catalog # U1330), 0.5 µlof 5 units µl−1 Taq polymerase (Promega, Madison,WI. Catalog # M1665), 1 µl each of 10nM upstreamand downstream primer (synthesized by OperonTechnologies, Inc., Alameda, CA) and 69.0 µl of0.02um filter sterilized autoclaved water. The PCRamplification profile was; one cycle for 2 minutes at94 ◦C, 40 cycles of [30 seconds at 94 ◦C, 30 secondsat 45 ◦C, 2 minutes at 72 ◦C], one cycle of 10 minutesat 72 ◦C and hold at 4 ◦C. PCR amplicons werecleaned and sequenced (one strand, one reaction)by Northwoods DNA, Inc. (Becida, MN). GenBankBlast search (http://www.ncbi.nlm.nih.gov/BLAST/)was used for amplicon/isolate identification.

2.4. Fungi identification

Fungi were identified to the genus level using micro-scopy or to the species level using 18S rDNAsequences as previously described (Griffin et al.2001b).

2.5. Statistical analysis

Dust and non-dust data sets were compared to deter-mine if there were significant differences in the respec-tive bacterial and fungal abundance values. Prior tothe use of parametric tests, a test of normality wasperformed on each raw data set using the Anderson-Darling test (D’Augostino and Stevens 1986; Shapiroand Francia 1972). The data sets that did not followa normal distribution were systematically transformedusing a series of transformation factors (e.g., log10)included in a ladder of powers program (Fry 1993) andagain tested for normality. The raw data sets that stilldid not follow a normal distribution following trans-formation were compared using the non-parametricMann-Whitney two sample rank test (Sokal and Rohlf1981). All tests were performed at an α = 0.05 usingMinitab (rel. 13) (Minitab, Inc., State College, PA).

2.6. GenBank Accession numbers

Accession numbers for the sequences of 2001 Africandust event isolates included in this project areAY278865 through AY278943.

3. Results

Table 1 lists the results of atmospheric samples takenfrom 18 July 2000 to 8 August 2001. The year2000 non-dust samples contained an average of 0.048culturable microbes L−1 (bacteria and fungi) of airsampled compared to the samples taken during dustevents which contained an average of 0.249 culturablemicrobes L−1 (5.2 times the non-dust concentration).The year 2001 non-dust samples contained an aver-age of 0.011 culturable microbes L−1 compared tothe 2001 dust samples, which contained an averageof 0.053 cultivable microbes L−1 (4.9 times the non-dust concentration). The total overall volume of airsampled during non-dust conditions of both years was3652 L, which resulted in the recovery of 47 culturablebacteria and fungi. During African dust events a totalof 2369 L of air were filtered, from which 247 colo-nies of bacteria and fungi were recovered. The overall

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averages of microbes L−1 of air sampled was 0.013for non-dust and 0.105 for dust resulting in a recoveryrate during dust conditions which was 8.0 times that ofnon-dust.

These data were compared for equivalence usingthe non-parametric Mann-Whitney test (α = 0.05) asneither data set followed a normal distribution, regard-less of the transformation used. Median values for thenon-dust and dust samples were 0.003 microbes L−1

and 0.067 microbes L−1 respectively. The resultingconfidence interval was 95.2% with P-values of 0.016and 0.013 when adjusted for ties.

Four periods of dust samples are represented inTable 1, three of which occurred during the normaldust season (May through October) and one, whichwas collected in the off-season (April). The highestrates of microbial recovery, 0.402 L−1 and 0.274 L−1

occurred during dust events in late July and August of2000 and 2001, respectively.

Table 2 lists data from sample taken during theJuly 30th, 2001 dust event. A total of 9 bacteria (n =10) and 5 fungi (n = 6) were identified from the ori-ginal sample. All the bacterial colonies recovered weregram + bacteria and one of the isolates was Bacillusthuringiensis, a known pathogen of insects (Helgasonet al. 2000; Yang et al. 2003). Six of the nine identifiedbacterial colonies were Bacillus sp. The majority ofisolated fungi were Cladosporium sp.

Table 3 lists the data for the three samples collec-ted during the dust event on 8 August 2001. Sixty-twobacteria (n = 73) and 36 fungi (n = 48) were identifiedfrom the original sample. Of the 62 identified bacteria,33 were gram + (57%, accounting for the 5 unknownslisted in Table 3) and 24 were gram negatives. Ofthe 24 isolates identified to the species level, four areknown pathogens (three colonies of Microbacteriumarborescens, and the Pseudomonas aeruginosa). Ofthe fungi identified, 11 were Cladosporium sp., 7were Aspergillus sp., 7 were Penicillium sp., 4 wereMicrosporium sp., 3 were Bipolaris sp., 2 were Pae-cilomyces sp. and 2 isolates of the genera Acremoniumand Nigrospora.

Table 4 lists the results of the samples collectedaboard ship during the June and July cruises of 2001.Note that the air was clear of African dust duringboth cruises, however there were some instances ofhumidity haze. Of the identified bacteria (n = 14)and fungi (n = 15), 3 were laboratory contaminates(June cruise – the Nigrospora sp. isolate, July cruise– the Sphingomonas sp. and Streptomyces sp. isol-ates). Of the bacteria isolates (n = 12) collected from

the atmospheric samples, 2 were gram + (17%). Thetwo laboratory bacterial contaminates recovered fromthe negative control plates were gram + and gram –isolates, respectively. No contamination was observedon any of the other negative control plates. Duringthe June cruise, the nine identified atmospheric fungiisolates included 2 colonies of Cladosporium sp., 2colonies of Microsporium sp., and 1 colony each ofChrysosporium sp., Penicillium sp., Rhizomucor sp.,Scytalidium sp. and Trichophyton sp.

4. Discussion

Table 1 lists viable counts of all samples collectedbetween July 18, 2000 and August 8, 2001. Dur-ing that time period two dust events occurred duringwhich a statistically significant greater number of cul-turable microorganisms were recovered. Abundancesof microorganisms during these two events rangedin the tenths to hundredths per liter. The only non-dust sample which was within this range occurredon July 18, 2000. While it was noted visually thatno dust was present in the area during sampling,the National Aeronautics and Space Administrations(NASA) Earth Probe satellite’s Total Ozone MappingSpectrophotometer (TOMS) shows aerosol activity inthe region three days prior on July 15, 2000 (forinformation on TOMS, which can detect atmospheri-cally suspended particles such as dust, smoke and ash,visit http://jwocky.gsfc.nasa.gov) (Torres et al. 1998;Hsu et al. 1999). TOMS images taken on the dayof sampling and the following 2 days shows aerosolsapproaching and impacting the Caribbean field sta-tions. It should be stated that the TOMS aerosol indexis not good below 1 km in the atmosphere, whichmay limit the ability to detect the leading or trailingedges of individual dust events (although TOMS aero-sol optical depth has near-surface resolution duringcloud free conditions) (Torres et al. 1998; Hsu et al.1999). We have noted at another of our field sites thatas a dust cloud moves through a region it can leavesuspended residual particle’s such as fine inorganicsand microorganisms that typically takes two to threedays to clear (manuscript in preparation). Also notedin Table 1 is that the dust events, which occurredin April of 2000 and early July of 2001, resultedin no or a negligible number (maximum of two persample) of microbes recovered. This could be due totemporal differences in dust cloud origin or physicalstresses (UV, temperature, desiccation, etc.) on the

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Table 2. Isolates identified from an air sample collected on July 30, 2001, during a dust event. This sample was collected offshore, upwind ofLittle St. James Island, USVI, using a small boat

Microorganism Classification Identified # matched bases Comments

(% DNA

homology)

30 July 2001

Bacillus pumilus Bacteria/Gram + 4 669/675(98) Potential human pathogen and common environmental

606/606(100) isolate (Banerjee et al. 1988; Hoult and Tuxford 1991)

602/606(99)

468/468(100)

Bacillus thuringiensis Bacteria/Gram + 1 566/568(99) Insect pathogen. Used as a mosquito control agent.

Common soil isolates (Chen et al. 2002; Yang et al. 2003)

Microbacterium Bacteria/Gram + 1 664/667(99) Species of this genus commonly isolated in environmental

imperiale studies (Arrault et al. 2002; Dutkiewicz et al. 2002)

Propionibacterium sp. Bacteria/Gram + 1 466/473(98) Id’d same to many species in this genus, 3 of 7 matches

were P. acnes a known human pathogen (Eady et al. 2003)

Unknown Bacteria/Gram + 1 651/655(99) Match at 99% to Bacillus barbaricus (628/633)

Aureobasidium sp. Fungi 1 N/A Common temperate-climate plant leaf isolates. Can

cause skin infections. Rare cases of systemic infection

in immunocompromised patients (St-Germain 1996)

Cladosporium sp. Fungi 4 N/A Common environmental isolates, plant and human

pathogenic species (St-Germain 1996)

Trichophyton sp. Fungi 1 N/A 11 human and 4 animal hair, scalp, and skin pathogens of

22 known species (St-Germain 1996)

transported microbial communities (Imshenetsky et al.1978; Gloster et al. 1982). The variability in microbesrecovered at the three different time points duringthe dust event on August 8, 2001 clearly demon-strates the temporal and spatial heterogeneity of boththe dust itself and the microbes it carries. The twocruise studies demonstrated that it is not unusual tofind viable microorganisms in the atmosphere over theocean. Another interesting cruise result was that thehighest abundance of microorganisms (eight bacteriaand 1 fungi on June 8, 2001) occurred when the skywas hazy. This haze was due to high humidity andmay have served to keep aerosolized marine micro-organisms (generated via sea spray) suspended in theair longer than normal. This may explain the highnumbers of gram – bacteria collected during the twocruise sample periods (gram – bacteria are common tomarine waters).

Figure 1 is a SeaWifs satellite image of August8, 2001 and shows dust activity across the tropical

Atlantic for that time period. As can be seen in Tables2 (July 30, 2001) and 3 (August 8, 2001), a numberof these bacterial or fungal isolates are closely relatedto microorganisms typically found in soils or in asso-ciation with plant life (Smit et al. 1999; Tsavkelova etal. 2001; Mecalfe et al. 2002). The most frequentlyrecovered fungi were Cladosporium sp. This genusof fungi is one of the most frequently recovered inenvironmental field studies and many species withinthis genus are pathogens to a wide variety of plantsand animals (Banerjee et al. 2002; Kantarcioglu etal. 2002; Mezzari et al. 2002). Other fungi recoveredduring these sample periods include Aspergillus sp.,Acremonium sp., Aureobasidium sp., Bipolaris sp.,Microsporium sp., Nigrospora sp., Paecilomyces sp.and Penicillium sp. Outside of Aspergillus sp., ofwhich 20 are known pathogenic human species (St-Germain 1996), most of the others are usually found insoils or in association with plants and in rare cases maycontain species that cause opportunistic human infec-

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Table 3. Identified isolates collected on August 8, 2001, from Deck Point, St. Thomas, USVI during an African dust event

Microorganism Classification # isolatesidentified

# matchedbases(% DNAhomology)

Comments

Actinosynnemamirum

Bacteria/Gram + 1 629/644(97) Antibiotic producing soil isolate (Watanabe et al. 1983)

Afipia genosp. 11 Bacteria/Gram – 1 482/499(96) Species identified in human disease surveillance studies/pathogen(Lappin 1993; Giladi et al. 1998)

Agrococcus jenensis Bacteria/Gram + 1 472/480(98) NW China semi-arid/arid legume isolate (information from Gen-Bank match submission data) and (Groth et al. 1996)

Ancylobacter sp. Bacteria/Gram – 1 573/605(94) Species identified in soils, water and bioremediation studies(Fulthorpe and Allen 1995)

Arthrobacterchlorophenolicus

Bacteria/Gram + 1 613/640(95) Has been used to degrade 4-chlorophenol in soils (Westerberg et al.2000)

Arthrobacter sp. Bacteria/Gram + 1 417/433(96) Id’d equally to A. ramosus and A. pascens. Soil isolate (informationfrom GenBank match submission data)

Bacillus sp. Bacteria/Gram + 1 671/693(96) Id’d equally to B. cereus and B. thuringiensis (insect pathogen).Common soil isolates (Jager et al. 2001; Tsavkelova et al. 2001;Yang et al. 2003)

Bosea thiooxidans Bacteria/Gram – 1 647/676(95) Denitrifying bacteria, can degrade phenol (Das et al. 1996)

Curtobacterium sp. Bacteria/Gram + 3 533/534(99),506/521(97),576/577(99)

Id’d equally to C. citreum and C. albidum in all cases. C. citreumidentified in a study of African centipede feces (Oravecz et al. 2002)

Curtobacteriumluteum

Bacteria/Gram + 1 691/697(99) Soil isolate (information from GenBank match submission data)

Curtobacteriumalbidum

Bacteria/Gram + 1 526/536(98) Rice isolate (information from GenBank match submission data)

Frankiaceae Bacteria/Gram + 1 680/709(95) Soil isolate (information from GenBank match submission data)

Fulvimaria litoralis Bacteria/Gram – 1 621/657(94) Marine isolate (information from GenBank match submission data)

Hymenobacter sp. Bacteria/Gram – 1 447/466(95) Spacecraft assembly building air isolate (information from Gen-Bank match submission data)

Kocuriaerythromyxa

Bacteria/Gram + 1 651/669(97) Marine isolate (information from GenBank match submission data)

Kocuria sp. Bacteria/Gram + 1 674/694(97) Human noma lesion isolate (Paster et al. 2002)

Kocuria sp. Bacteria/Gram + 1 545/551(98) Id’d equally to K. polaris and K. erythromyxa

Kineococcus-like Bacteria/Gram + 1 673/687(97) Mojave desert isolate (information from GenBank match submis-sion data)

Mesorhizobium sp. Bacteria/Gram – 1 699/719(97) Plant isolate (Ba et al. 2002)

Microbacteriumarborescens

Bacteria/Gram + 3 534/538(98),697/708(98),576/579(99)

Noma lesion and soil isolates (Dutkiewicz et al. 2002; Paster et al.2002).

Microbacteriumtestaceum

Bacteria/Gram + 1 572/576(99) Soil isolate (information from GenBank match submission data).

Microbacteriumtrichotecenolyticum

Bacteria/Gram + 1 650/660(98) Soil isolate (information from GenBank match submission data).

Microbacterium sp. Bacteria/Gram + 2 560/568(98),778/784(99),519/549(94)

Soil isolates (information from GenBank match submission data).

Nocardioides sp. Bacteria/Gram + 1 663/672(98) Can metabolize the herbicide S-triazine (Mulbry et al. 2002)

Paracoccus sp. Bacteria/Gram – 2 548/564(97),606/618(98),549/560(98)

Marine and spacecraft assembly building isolates (information fromGenBank match submission data)

Propionibacteriumsp.

Bacteria/Gram + 1 534/539(99) Id’d same to many species in this genus, most P. acnes a knownhuman pathogen (Paster et al. 2002)

Pseudomonasaeruginosa

Bacteria/Gram – 1 417/417(100) Human pathogen (Poole and McKay 2003)

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Table 3. Continued

Microorganism Classification # isolatesidentified

# matchedbases(% DNAhomology)

Comments

Rhizobiumyanglingense

Bacteria/Gram – 1 699/729(95) NW China semi-arid/arid legume isolate (Tan et al. 2001)

Rhizobium sp. Bacteria/Gram – 1 458/471(96) Found in arid regions (Gao et al. 2002)

Saccharothrixtexasensis

Bacteria/Gram + 2 562/563(99),506/508(99)

Soil isolate (information from GenBank match submission data)

Sphingomonasechiniodes

Bacteria/Gram – 1 624/647(96) Common environmental isolates (information from GenBank matchsubmission data)

Sphingomonas mali Bacteria/Gram – 1 625/638(97) Common environmental isolates (information from GenBank matchsubmission data)

Sphingomonaspaucimobilis

Bacteria/Gram – 2 481/494(97),616/641(96)

Chloropenol and PAH degrading isolates respectively. Potentialhuman pathogen (de Otero et al. 1998)

Sphingomonaswittichii

Bacteria/Gram – 1 490/513(95) Can metabolize dibenzo-p-dioxin (Yabuuchi et al. 2001)

Sphingomonas sp. Bacteria/Gram – 4 511/529(96),501/519(96),461/478(96),526/542(97)

Nigerian noma lesion isolate, A/C biofilm isolate, soil isolate andAntarctic gypsum crust isolate respectively (Paster et al. 2002)(information from GenBank match submission data)

Streptomyces sp. Bacteria/Gram + 5 707/713(99),579/583(99),500/506(98),562/568(98),717/769(93)

Common environmental isolates. > 97% homology matchedequally to many species (S. thermotolerans and S. bellus are acouple) A major source of antibiotics and some species are patho-genic. (Chater 1999; Toth et al. 2001; Elzein et al. 2002)

Taxeobactergelupupurascens

Bacteria/Gram – 1 644/659(97) Antarctic soil isolate (information from GenBank match submissiondata)

Unknown Bacteria/Gram – 1 626/644(97) Uncultured alpha Proteobacteria – soil DNA (information fromGenBank match submission data)

Unknown Bacteria/Gram – 1 662/683(96) Uncultured beta Proteobacteria – soil DNA (information fromGenBank match submission data)

Unknown Bacteria/Gram + 2 661/676(97),599/616(97)

Also matched at 97% to Sphingomonas sp. (information fromGenBank match submission data)

Unknown Bacteria/Gram – 1 572/583(95) Close match with the Genus Roseomonas (information from Gen-Bank match submission data)

Unknown Bacteria 5 400/419(95),337/358(94),572/583(98),640/678(94),560/580(96)

Unidentified, marine manganese-oxidizing, isolate from cysticfibrosis patient, potato isolate and soil isolate respectively (infor-mation from GenBank match submission data)

Acremonium sp. Fungi 1 N/A Common soil and plant isolate. Some reported cases of humandisease (St-Germain 1996)

Aspergillus sp. Fungi 7 N/A Common soil and plant isolate. Over 20 species recognized asopportunistic human pathogens. Species also pathogens to birds andmammals (St-Germain 1996)

Bipolaris sp. Fungi 3 N/A Common soil and plant isolate in the tropics and subtropics. Canoccasionally cause disease in humans but primarily recognized as aplant pathogen (St-Germain 1996)

Cladosporium sp. Fungi 11 N/A Common environmental isolate, plant and human pathogenic spe-cies (St-Germain 1996)

Microsporium sp. Fungi 4 N/A 5 human and 7 animal pathogens of 17 known species. Skin and hairinfections (St-Germain 1996)

Nigrospora sp. Fungi 1 N/A Common plant and soil isolate (St-Germain 1996)Paecilomyces sp. Fungi 2 N/A Common soil and plant isolate. Rare human pathogen and some

species identified as insect pathogens (St-Germain 1996)Penicillium sp. Fungi 7 N/A Common temperate-climate isolates. P. marneffie can cause lympha-

tic infections (St-Germain 1996)

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Table 4. Non-dust isolates identified from samples collected in the northern Caribbean during the June and July cruises, on the “Explorer ofthe Seas”

Genus/species Type # isolates # matched bases(% homology)

Information

June Cruise (June 2nd through the 9th, 2001)

Acinetobacter sp. Bacteria/Gram – 3 540/541(99),537/537(100),482/486(99)

Common environmental soil and water isolates. Id’dequally to A. johnsonii, junii, anitratus, etc. (informationfrom GenBank match submission data)

Afipia genosp. 11 Bacteria/Gram – 1 499/518(96) Human isolate/pathogen (Lappin 1993; Giladi et al.1998)

Duganella sp. Bacteria/Gram – 1 699/706(99) Beta Proteobacteria. Genus DNA has been identifiedin human disease studies (information from GenBankmatch submission data)

Propionibacterium sp. Bacteria/Gram + 1 369/379(97) Id’d same to many species in this genus, most P. acnes aknown human pathogen (Eady et al. 2003)

Pseudomonas sp. Bacteria/Gram – 4 473/478(98),482/486(99),697/701(99),377/378(99),611/613(99)

Common environmental soil and water isolates(information from GenBank match submission data)

Sphingomonas sp. Bacteria/Gram – 1 657/677(97) Id’d to S. pruni and S. aquatilis. Common environmentalisolate. S. pruni is a plant pathogen (information fromGenBank match submission data)

Chrysosporium sp. Fungi 1 N/A Common plant and soil isolate. Rare cases of humanpathogenicity (St-Germain 1996)

Cladosporium sp. Fungi 2 N/A Common environmental isolate, plant and human patho-genic species (St-Germain 1996)

Microsporium sp. Fungi 2 N/A 5 human and 7 animal pathogens of 17 known species.Skin and hair infections (St-Germain 1996)

Nigrospora sp. Fungi 1 N/A Lab. Contaminate. Common plant and soil isolate (St-Germain 1996)

Penicillium sp. Fungi 1 N/A Common temperate-climate isolate. P. marneffie cancause lymphatic infections (St-Germain 1996)

Rhizomucor sp. Fungi 1 N/A Common environmental isolate. R. pusillus can causeinfections in the immunocompromised (St-Germain1996)

Scytalidium sp. Fungi 1 N/A Common tropical plant and soil isolate (St-Germain1996)

Trichophyton sp. Fungi 1 N/A 11 human and 4 animal hair, scalp, and skin pathogensof 22 known species (St-Germain 1996)

July Cruise (July 21st through the 28th, 2001)

Bacillus megaterium Bacteria/Gram + 1 522/523(99) Tree pathogen (Barnard and Dixon 1983)

Sphingomonas sp. Bacteria/Gram – 1 428/435(98) Laboratory contaminate. Common environmental isolate(information from GenBank match submission data)

Streptomyces sp. Bacteria/Gram + 1 654/659(99) Laboratory contaminate. Id’d equally toS. thermotolerans and S. bellus

Microsporium sp. Fungi 1 N/A 5 human and 7 animal pathogens of 17 known species.Skin and hair infections (St-Germain 1996)

Trichophyton sp. Fungi 4 N/A 11 human and 4 animal hair, scalp, and skin pathogensof 22 known species (St-Germain 1996)

154

tions (St-Germain 1996). A number of the bacterialisolates matched to GenBank sequences of knownpathogens or isolates identified in human disease sur-veillance studies (Stone and Whitehead 1970; Pasteret al. 2002). A number of isolates identified simi-larly to sequences found in a Nigerian noma lesionstudy to include; the Kocuria sp. isolate at 97%, theMicrobacterium arborescens isolate at 98%, and theSphingomonas sp. isolate at 96% (Paster et al. 2002).Pseudomonas aeruginosa is an opportunistic pathogenthat can cause fatal infections in burn patients (Stoneand Whitehead 1970). One of the unknown bacteriaidentified at 98% sequence similarity to an isolatefrom a cystic fibrosis patient (GenBank accession #– AY043384.1). Several of the isolates matched tomicroorganisms previously identified in arid or desertenvironments, including Agrococcus jenensis (NWChina legume isolate), the Kineococcus-like isolate(matched at 97% to a GenBank Mojave desert isolate– accession # AF060691), and Rhizobium yanglin-gense (NW China legume isolate) (Tan et al. 2001).Two of the isolates matched to isolates collected fromthe atmosphere within a spacecraft assembly build-ing in another aeromicrobiology study (Hymenobactersp. and Paracoccus sp., unpublished Genbank sub-mission data. AF408274 and AY167832 accession #’srespectively) and a number of isolates matched orga-nisms previously shown to degrade soil pollutants suchas polyaromatic hydrocarbons (A. chlorophenolicus,Nocardioides sp., S. paucimobilis, and S.wittichii)(Westerberg et al. 2000; Yabuuchi et al. 2001; Mulbryet al. 2002).

It should be noted that the USVI microbial isol-ates collected during non-dust conditions in generalrepresent background levels of microorganisms (aero-solized via terrestrial disturbances). This can be seenin many of the USVI non-dust samples where atleast one colony of bacteria or fungi were recoveredin 50% of those samples (Table 1). This data indi-cates that while collecting airborne microorganismsduring African dust events, a few “local” microorga-nisms may be collected simultaneously with the for-eign flora. Although the field of microbial ecology islimited in its ability to distinguish foreign from localflora (some progress has been made (Cho and Tiedje2000)), we are currently identifying all culturable isol-ates in order to develop a database which in timemay allow us to identify regionally specific groups orisolates within pure or mixed samples.

Table 4 lists the results of the non-dust offshoresamples collected during the June and July cruises.

The genus of fungi that was most often recoveredwas the Trichophyton sp. Fifteen of twenty-two knownTrichophyton species are known pathogens to humansand other animals (St-Germain 1996). Three isolatesof Microsporium (5 human and 7 animal pathogensof the 17 known species) (St-Germain 1996) wereisolated during the two cruises, followed by the twocolonies of Cladosporium sp. collected on the Junecruise. Other fungi collected included Chrysosporiumsp., Penicillium sp., Rhizomucor sp., Scytalidium sp.and Trichophyton sp. Of the bacteria collected, isolatesof Acinetobacter sp. and Pseudomonas sp. (gram –bacteria) were the most commonly encountered. Spe-cies of theses two genera are commonly found inaquatic and soil environments and may represent thepresence of aerosolized marine organisms moving inthe near sea-surface atmosphere due to surface acti-vity (sea spray) (Maynard 1968). Bacillus megateriumis a known tree pathogen and one isolate was collec-ted during the July cruise (Barnard and Dixon 1983).The Duganella sp. isolate matched at 99% sequencesimilarity to DNA isolated from human tissue duringa disease surveillance study (Tanner et al. 1998).

The cruise isolates are predominantly gram – richin contrast to the predominantly gram + rich late sum-mer USVI isolates. As previously stated, the majorityof late summer isolates (all of the gram + isolates)were either high G+C content gram + or low G+Cspore forming gram +. High G+C content DNA or theability to form spores (bacteria and fungi) are traitswhich impart resistance to UV inactivation (Singerand Ames 1970; Riesenman and Nicholson 2000;Setlow 2001). The late summer dust community iden-tified in this study could represent a fingerprint of amicrobial community that has been exposed to peri-ods of physical stress (UV exposure, desiccation, hightemperature) which is not conducive to microbial sur-vival. Although a large number of bacteria were of thetype typically resistant to UV stress, a large fraction(∼40%) were gram – bacteria. These bacteria mayrepresent sea-spray bacteria, which were picked up bythe trade winds and transported with the dust clouds,or simply soil isolates that survived the usual 5 to 7day transoceanic journeys. In addition to UV inducedstress other factors that have been identified to play arole in airborne microbial survival are desiccation andtemperature (Gloster et al. 1982; Lysenko and Demina1992). We believe that transoceanic transport exposesthe dustborne microorganisms to more moderate tem-peratures and humidity than would typically be foundover land and would favor microbial survival. Another

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factor that may influence transoceanic survival is thatmicrobes at lower altitudes within these dust cloudswill also receive lower UV exposures due to the fil-tering effect of the upper layers of any individualdust cloud. Studies have shown that UV attenuationthrough dust clouds can be as high as 50% (Herman etal. 1999). Inorganic or organic microbe-laden particleswithin these clouds will also provide some degree ofUV shielding as the particles tumble during transit.

We have previously reported that during Africandust events the numbers of culturable microbesrecovered in the USVI could be 2–3 times greaterthan those seen during non-dust conditions (Griffinet al. 2001a). In this study we found that on averagethere was an 8-fold increase in the number of cul-turable microorganisms during dust events, relative tonon-dust events. What is clear is that many differenttypes of microorganisms survive the airborne trip fromAfrica to the Caribbean and Americas and there isconsiderable temporal and spatial variation in species.These mobile communities may serve as seed to downwind ecosystems over vast distances. This mechanismof transoceanic dispersion of both non-pathogenic andpathogenic microorganisms may play a significant rolein ecological change through time and environmentalhealth.

Acknowledgments

This research was funded by a grant from the NationalAeronautics and Space Administration’s, Earth Sci-ence and Public Health Program, grant # 7242-60050.Thanks to the US National Park Service (Denver, CO)for the St. John, USVI wind-speed and wind-directiondata. Special thanks to the University of Miami forthe use of the ship laboratories and personnel supportduring our at sea atmospheric studies aboard RoyalCaribbean’s “Explorer of the Seas”. For informationon research aboard “Explorer of the Seas” please visithttp://www.rsmas.miami.edu/rccl/.

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