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Ejection of microalgae into the air via bursting bubbles
BRIEF COMMUNICATION
Ejection of microalgae into the air via bursting bubbles Harold
E. Schlichting,
Jr. Port Sanilac, Mich.
Air bubbles bursting at the water surface can ejeot as 13 om. Because these organisms have been reported piratory allergic disease, this mechanism is suggested neroallergens.
lnioroa1ga.e into the air as high as cawsattie organisms in resa.s a potential source of these
Woodcocks suggested that aerosols are formed by bubbles bursting from breaking waves and that microorganisms 0.3 to 30 P in diameter in atmospheric water droplets could be dispersed by air currents. A bursting bubble 0.3 to 4.3 cm. in diameter ejects 4 or 5 droplets about 3s its size and a second set 5 to 30 ~1.’ Every second more than 100,000 bursting bubbles form from a square meter of whitecap. The bubble jet droplets carry a minimum of 300 billion tons of seawater into the atmosphere each year. The first drop produced by the jet rises to heights of 19 cm. while the second rises only one-half that height.3 The height to which bubble jet droplets rise varies because of the organic material in the surface film.4 Microorganisms are concentrated in water surface film and in foams.5-Q Concentration in the surface film is usually more than 100 times greater than in the underlying water, and bubbling air through bacterial cultures increased the concentration of bacteria in the bubble jet droplets 2,000 times more than in the medium because of greater concentration in the surface film where the bubbles burst.3 .Jet droplets from a 600 p diameter bubble having a surface film 0.5 to 20 p thick are composed solely of surface film material.lO Ejection of bacteria into the air by the jet-bubble mechanisml’, I* contributes to public health problems.3vw-*’ Airborne microalgae have been shown to cause human allergies and respiratory difficulties associated with asthma-like attacks.1S-23However, few planktonic algae, fungi, or protozoans have been sampled from the atmosphere,24 and no studies have been reported that demonstrate the ejection of algae, fungi, or protozoans from the water surface into the air. Sterile air was bubbled through known microalgal cultures of depths 1 to 28 From the Department of Botany, North Carolina Received for publication April 23, 1973. Reprint requests to: Dr. Harold E. Schlichting, Jr., Mich. 48469.
State
University.
BioControl
Co., P. 0. Box Vol.
43, Port
Sanilac,
58, No. 3, pp. 185-188
186
Schlichting
TABLE
I. Ejection
J. ALLERGY
of 3 microalgae
by
bursting
CLIN.
IMMUNOL. MARCH 1974
bubbles
Bubbling rate/see.
CdlS/d.
Sample
Algae
1” 2 3 4 5 6 7
Braoteacooous Braateacoccws Oscillatoria Osdllatoria Stichococcus Stichoeooozls Stichococczcs
ii 10 11 12 ‘Sterile
TABLE
Stichococcus Stichocoecus Stichococcus Stichocoeeus agar
II. Algae
plates
ejected
were
*Exposure
time,
baoillaris baoillaris bacillaris bacillaris exposed
to
bubbles
Bubble size km.l
30 200 50
cultures
terestris (3 - 8 p) terestris (2 x 20 p) sp. hormogonia sp. hormogouia baoillark (2 x 4 G p) baoilluris baoillaris
by bursting
Bubbling de/sac.
in
0.75 0.75 0.5
bursting
from
bubbles,
aquariums Water
to plate km.)
4.5 7.0 4.5
2 cm.
in
of
culture
5.47 5.47 9.9 9.9 1.45 1.45 5.7
x x x x x x x
106 106 106 108 10’ 108 10’
. :1 *5 5 5 5 2 ix
5.7 5.7 5.7 5.7
x x x x
103 103 108 103 103
20 30 30 30 30
diameter,
from
cultures
in stores* Number ceils/plate
of
i: 1.600
5 minutes.
cm. for periods of 10 or 20 minutes at varying bubbling rates. All tests were run in triplicate in sterile plastic containers with no measurable air currents other than those caused by bubbling. Bacteria and fungi were ejected as high as 20 cm. while no algae were ejected to 20 cm., and only a Sew algal cells were ejected above 11 cm. The distance the bubble rose through the culture was not related to the number of cells ejected by the bursting bubble (Table I). When evaporation to dryness of a microalgal culture occurred in a sterile plastic container, the algae adhered to the container as a film. No algae were ejected to agar plates exposed at 2 cm. above the water surface. The ejection of microalgae into the a.ir over ten open aquariums in stores was also studied. Petri dishes of Bold’s basal medium agar were inverted 4.5 to 20 cm. above the water surfaces for 5 minutes. Bubble sizes were 0.5 to 8 cm., and the rate of bubbling was 1 to 400 bubbles per second. Visible water droplets 0.1 to 1 mm. were observed on some plates exposed as high as 11.5 cm. above the water surface (Table II). One bubble, traveling 18 cm. through the water, enlarged on the surface to 8 cm., burst, and ejected a minimum of 157 cells 7 cm. into the air. Chlorella minutissima (1.5 to 2.6 p) was the only alga in the aquarium water. Because microorganisms accumulate in the surface film and can be ejected into the air above aquariums, aerated aquarium water, visibly clean or clouded with microalgae, can be a health hazard. Sensitive individuals can suffer allergies and asthma-like attacks. Small light droplets are readily ejected into the air and transported by air
Of
VOLUME NUMBER
53 3
Ejection
Distance Exposure time
20 :o” 20 20 20 10 10 10 10 10 10
in
bubble culture (cm.1
1 1 1 1 1 1 28 28 17.5 17.5 s”::
traveled
Height of cell ejection km.)
8.0 11.0 8.0 11.0 8.0 11.0 5.5 13.0 5.5 13.0 1:::
of microalgae
into
number
the
air
187
Average of colonies
3.0 50::: 0 21.3 11.3 237.0 1 240.0 1 257.0 2
microalgae.
currents while larger droplets fall back into the water. When sampling the air collected the following genera near a sewage aeration tank in Texas, MahoneyI of bacteria : Aerobacter, Escherichia, Flavobacterium, Klebsiella, Micrococcus, Proteus, Pseudomonas, Salmonella, Sarcina, Serratia, and Staphylococcus. It would seem probable that when ejected from bursting bubbles in sewage aeration tanks, trickling filters, and fouled aquariums or fish tanks, droplets with microalgae may transport high concentrations of pathogenic bacteria and viruses into the air. Encouragement by Dr. I. L. Bernstein, Medical Center, University of Cincinnati, Ohio, manuscript review by Dr. L. A. Whitford, North Carolina State and assistance by D. R. Hill, Department of Biology, Belmont College, Nashville, are gratefully acknowledged.
Cincinnati, University, Tennessee,
REFERENCES 1 Woodcock, A. H.: Note concerning human respiratory irritation associated with high concentrations of plankton with mass mortality of marine organisms. J. Marine Res. 7: 56, 1948. 2 Mason, B. M.: Bursting of air bubbles at the surface of sea water, Nature 174: 470, 1954. 3 Blanchard, D. C., and Syzdek, L.: Mechanism for the water-to-air transfer and coneentration of bacteria, Science 170: 626, 1970. Blanchard, D. C.: The borderland of burning bubbles, Sat. Rev. 1: 60, 1972. Maynard, N. G.: Aquatic foams as an ecological habitat, Z. Allg. Mikrobiol. 8: 119, 1968. Parker, B. C., and Barsom, G.: Biological and chemical significance of surface microlayers in aquatic ecosystems, BioSci. 20: 87, 1970. Schlichting, H. E., Jr.: A preliminary study of the algae and protozoa in seafoam, Bot. Marina 14: 24, 1971. Bezdek, H. F., and Carlucci, A. F.: Surface concentrations of marine bacteria, Limnol. Oceanogr. 17: 566, 1972. 9 Loeb, G. I. (Naval Research Laboratory, Washington, D. C.) : Personal communication, 1972. 10 MacIntyre, F. : Bubbles : A boundary-layer “microtome” for micron-thick samples of a liquid surface, J. Phys. Chem. 72: 589, 1968. 11 Bezdek, H. F.: Size determination of sea water drops, J. Phys. Chem. 75: 3623, 1971. 12 Woodcock, A. H.: Bursting bubbles and air pollution, Sewage and Industrial Wastes 27: 1189, 1955. 13 Mahoney, J. L.: A qualitative survey of the airborne algae, protozoa and bacteria at the Denton sewage treatment plant, M.S. thesis, North Texas State University, 1968. 14 Wolfe, H. W.: Sampling microbiological aerosols, Public Health Service Bull., p. 686, 1959.
188
J. ALLERGY
Schlichting
CLIN.
IMMUNOL. MARCH 1974
15 Ledbetter, J. 0.: Air pollution from aerobic waste treatment, Water and Sewage Works 111: 62, 1964. 16 Napalitano, P. J., and Rowe, D. R.: Microbial content of air near sewage treatment plants, Water and Sewage Works 113: 480, 1966. 17 Adams, A. P., and Spendlove, J. C.: Coliform aerosols emitted by sewage treatment plants, Science 169: 1218, 1970. 18 McElhenney, T. R., Bold, H. C., Brown, R. M., Jr., and McGovern, J. P.: Algae: A cause of inhalant allergy in children, Ann. Allergy 20: 739, 1962. 19 McGovern, J. P., Haywood, T. J., and McElhenney, T. R.: Airborne algae and their allergenicity. II. Clinical and laboratory multiple correlation studies with four genera, Ann. Allergy 24: 145, 1966. 20 Bernstein, I. L., and Safferman, R. S.: Sensitivity of skin and bronchial mucosa to green algae, J. ALLERGY 38: 166, 1966. 21 Bernstein, I. L., and Safferman, R. S.: Viable algae in house dust, Nature 227: 851, 1970. 22 Bernstein, I. L., and Safferman, R. S.: A model system for studying the aerobiology and U.S./I.B.P. Aerobiology Program Handbook No. 3, biomedical impact of green algae, University of Michigan, Ann Arbor, p, 156, 1973. 23 Benaim-Pinto, C. : Airborne algae as a possible etiologic factor in respiratory allergy in Caracas, Venezuela, J. ALLERGY 49: 356, 1972. (Correspondence.) 24 Schlichting, H. E., Jr.: The importance of airborne algae and protozoa, Air Pollution Control J. 19: 945, 1969.
Answers The
correct
for
Allergy answers
Foundation
of
America
to questions
in this
Journal
Self-Assessment issue
are
Program as
follows:
Question
1 Ip.
149):
B, see Sheldon, J. M., et al.: allergy, ed. 2, Philadelphia, Company, p. 203.
A manual 1967, W.
Question
2 (p.
157):
C, see Freedman, S. York, 1971, Harper
Question
3 (p.
169):
D, see diPalma, J. R., editor: Drill’s Pharmacology medicine, ed. 4, New York, 1971, Blakiston sion, McGraw-Hill Book Company, p. 533.
1
of clinical B. Saunders
/ I
0.: Clinical immunology, New & Row, Publishers, p. 352.
1
in Divi-
1 I I
see Szentivanyi, A.: The beta adrenergic theory of the atopic abnormality in bronchial asthma, J. Allergy, 42: 203-232, 1968.
i 1 I
Ejection of microalgae into the air via bursting bubbles Harold
E. Schlichting,
Jr. Port Sanilac, Mich.
Air bubbles bursting at the water surface can ejeot as 13 om. Because these organisms have been reported piratory allergic disease, this mechanism is suggested neroallergens.
lnioroa1ga.e into the air as high as cawsattie organisms in resa.s a potential source of these
Woodcocks suggested that aerosols are formed by bubbles bursting from breaking waves and that microorganisms 0.3 to 30 P in diameter in atmospheric water droplets could be dispersed by air currents. A bursting bubble 0.3 to 4.3 cm. in diameter ejects 4 or 5 droplets about 3s its size and a second set 5 to 30 ~1.’ Every second more than 100,000 bursting bubbles form from a square meter of whitecap. The bubble jet droplets carry a minimum of 300 billion tons of seawater into the atmosphere each year. The first drop produced by the jet rises to heights of 19 cm. while the second rises only one-half that height.3 The height to which bubble jet droplets rise varies because of the organic material in the surface film.4 Microorganisms are concentrated in water surface film and in foams.5-Q Concentration in the surface film is usually more than 100 times greater than in the underlying water, and bubbling air through bacterial cultures increased the concentration of bacteria in the bubble jet droplets 2,000 times more than in the medium because of greater concentration in the surface film where the bubbles burst.3 .Jet droplets from a 600 p diameter bubble having a surface film 0.5 to 20 p thick are composed solely of surface film material.lO Ejection of bacteria into the air by the jet-bubble mechanisml’, I* contributes to public health problems.3vw-*’ Airborne microalgae have been shown to cause human allergies and respiratory difficulties associated with asthma-like attacks.1S-23However, few planktonic algae, fungi, or protozoans have been sampled from the atmosphere,24 and no studies have been reported that demonstrate the ejection of algae, fungi, or protozoans from the water surface into the air. Sterile air was bubbled through known microalgal cultures of depths 1 to 28 From the Department of Botany, North Carolina Received for publication April 23, 1973. Reprint requests to: Dr. Harold E. Schlichting, Jr., Mich. 48469.
State
University.
BioControl
Co., P. 0. Box Vol.
43, Port
Sanilac,
58, No. 3, pp. 185-188
186
Schlichting
TABLE
I. Ejection
J. ALLERGY
of 3 microalgae
by
bursting
CLIN.
IMMUNOL. MARCH 1974
bubbles
Bubbling rate/see.
CdlS/d.
Sample
Algae
1” 2 3 4 5 6 7
Braoteacooous Braateacoccws Oscillatoria Osdllatoria Stichococcus Stichoeooozls Stichococczcs
ii 10 11 12 ‘Sterile
TABLE
Stichococcus Stichocoecus Stichococcus Stichocoeeus agar
II. Algae
plates
ejected
were
*Exposure
time,
baoillaris baoillaris bacillaris bacillaris exposed
to
bubbles
Bubble size km.l
30 200 50
cultures
terestris (3 - 8 p) terestris (2 x 20 p) sp. hormogonia sp. hormogouia baoillark (2 x 4 G p) baoilluris baoillaris
by bursting
Bubbling de/sac.
in
0.75 0.75 0.5
bursting
from
bubbles,
aquariums Water
to plate km.)
4.5 7.0 4.5
2 cm.
in
of
culture
5.47 5.47 9.9 9.9 1.45 1.45 5.7
x x x x x x x
106 106 106 108 10’ 108 10’
. :1 *5 5 5 5 2 ix
5.7 5.7 5.7 5.7
x x x x
103 103 108 103 103
20 30 30 30 30
diameter,
from
cultures
in stores* Number ceils/plate
of
i: 1.600
5 minutes.
cm. for periods of 10 or 20 minutes at varying bubbling rates. All tests were run in triplicate in sterile plastic containers with no measurable air currents other than those caused by bubbling. Bacteria and fungi were ejected as high as 20 cm. while no algae were ejected to 20 cm., and only a Sew algal cells were ejected above 11 cm. The distance the bubble rose through the culture was not related to the number of cells ejected by the bursting bubble (Table I). When evaporation to dryness of a microalgal culture occurred in a sterile plastic container, the algae adhered to the container as a film. No algae were ejected to agar plates exposed at 2 cm. above the water surface. The ejection of microalgae into the a.ir over ten open aquariums in stores was also studied. Petri dishes of Bold’s basal medium agar were inverted 4.5 to 20 cm. above the water surfaces for 5 minutes. Bubble sizes were 0.5 to 8 cm., and the rate of bubbling was 1 to 400 bubbles per second. Visible water droplets 0.1 to 1 mm. were observed on some plates exposed as high as 11.5 cm. above the water surface (Table II). One bubble, traveling 18 cm. through the water, enlarged on the surface to 8 cm., burst, and ejected a minimum of 157 cells 7 cm. into the air. Chlorella minutissima (1.5 to 2.6 p) was the only alga in the aquarium water. Because microorganisms accumulate in the surface film and can be ejected into the air above aquariums, aerated aquarium water, visibly clean or clouded with microalgae, can be a health hazard. Sensitive individuals can suffer allergies and asthma-like attacks. Small light droplets are readily ejected into the air and transported by air
Of
VOLUME NUMBER
53 3
Ejection
Distance Exposure time
20 :o” 20 20 20 10 10 10 10 10 10
in
bubble culture (cm.1
1 1 1 1 1 1 28 28 17.5 17.5 s”::
traveled
Height of cell ejection km.)
8.0 11.0 8.0 11.0 8.0 11.0 5.5 13.0 5.5 13.0 1:::
of microalgae
into
number
the
air
187
Average of colonies
3.0 50::: 0 21.3 11.3 237.0 1 240.0 1 257.0 2
microalgae.
currents while larger droplets fall back into the water. When sampling the air collected the following genera near a sewage aeration tank in Texas, MahoneyI of bacteria : Aerobacter, Escherichia, Flavobacterium, Klebsiella, Micrococcus, Proteus, Pseudomonas, Salmonella, Sarcina, Serratia, and Staphylococcus. It would seem probable that when ejected from bursting bubbles in sewage aeration tanks, trickling filters, and fouled aquariums or fish tanks, droplets with microalgae may transport high concentrations of pathogenic bacteria and viruses into the air. Encouragement by Dr. I. L. Bernstein, Medical Center, University of Cincinnati, Ohio, manuscript review by Dr. L. A. Whitford, North Carolina State and assistance by D. R. Hill, Department of Biology, Belmont College, Nashville, are gratefully acknowledged.
Cincinnati, University, Tennessee,
REFERENCES 1 Woodcock, A. H.: Note concerning human respiratory irritation associated with high concentrations of plankton with mass mortality of marine organisms. J. Marine Res. 7: 56, 1948. 2 Mason, B. M.: Bursting of air bubbles at the surface of sea water, Nature 174: 470, 1954. 3 Blanchard, D. C., and Syzdek, L.: Mechanism for the water-to-air transfer and coneentration of bacteria, Science 170: 626, 1970. Blanchard, D. C.: The borderland of burning bubbles, Sat. Rev. 1: 60, 1972. Maynard, N. G.: Aquatic foams as an ecological habitat, Z. Allg. Mikrobiol. 8: 119, 1968. Parker, B. C., and Barsom, G.: Biological and chemical significance of surface microlayers in aquatic ecosystems, BioSci. 20: 87, 1970. Schlichting, H. E., Jr.: A preliminary study of the algae and protozoa in seafoam, Bot. Marina 14: 24, 1971. Bezdek, H. F., and Carlucci, A. F.: Surface concentrations of marine bacteria, Limnol. Oceanogr. 17: 566, 1972. 9 Loeb, G. I. (Naval Research Laboratory, Washington, D. C.) : Personal communication, 1972. 10 MacIntyre, F. : Bubbles : A boundary-layer “microtome” for micron-thick samples of a liquid surface, J. Phys. Chem. 72: 589, 1968. 11 Bezdek, H. F.: Size determination of sea water drops, J. Phys. Chem. 75: 3623, 1971. 12 Woodcock, A. H.: Bursting bubbles and air pollution, Sewage and Industrial Wastes 27: 1189, 1955. 13 Mahoney, J. L.: A qualitative survey of the airborne algae, protozoa and bacteria at the Denton sewage treatment plant, M.S. thesis, North Texas State University, 1968. 14 Wolfe, H. W.: Sampling microbiological aerosols, Public Health Service Bull., p. 686, 1959.
188
J. ALLERGY
Schlichting
CLIN.
IMMUNOL. MARCH 1974
15 Ledbetter, J. 0.: Air pollution from aerobic waste treatment, Water and Sewage Works 111: 62, 1964. 16 Napalitano, P. J., and Rowe, D. R.: Microbial content of air near sewage treatment plants, Water and Sewage Works 113: 480, 1966. 17 Adams, A. P., and Spendlove, J. C.: Coliform aerosols emitted by sewage treatment plants, Science 169: 1218, 1970. 18 McElhenney, T. R., Bold, H. C., Brown, R. M., Jr., and McGovern, J. P.: Algae: A cause of inhalant allergy in children, Ann. Allergy 20: 739, 1962. 19 McGovern, J. P., Haywood, T. J., and McElhenney, T. R.: Airborne algae and their allergenicity. II. Clinical and laboratory multiple correlation studies with four genera, Ann. Allergy 24: 145, 1966. 20 Bernstein, I. L., and Safferman, R. S.: Sensitivity of skin and bronchial mucosa to green algae, J. ALLERGY 38: 166, 1966. 21 Bernstein, I. L., and Safferman, R. S.: Viable algae in house dust, Nature 227: 851, 1970. 22 Bernstein, I. L., and Safferman, R. S.: A model system for studying the aerobiology and U.S./I.B.P. Aerobiology Program Handbook No. 3, biomedical impact of green algae, University of Michigan, Ann Arbor, p, 156, 1973. 23 Benaim-Pinto, C. : Airborne algae as a possible etiologic factor in respiratory allergy in Caracas, Venezuela, J. ALLERGY 49: 356, 1972. (Correspondence.) 24 Schlichting, H. E., Jr.: The importance of airborne algae and protozoa, Air Pollution Control J. 19: 945, 1969.
Answers The
correct
for
Allergy answers
Foundation
of
America
to questions
in this
Journal
Self-Assessment issue
are
Program as
follows:
Question
1 Ip.
149):
B, see Sheldon, J. M., et al.: allergy, ed. 2, Philadelphia, Company, p. 203.
A manual 1967, W.
Question
2 (p.
157):
C, see Freedman, S. York, 1971, Harper
Question
3 (p.
169):
D, see diPalma, J. R., editor: Drill’s Pharmacology medicine, ed. 4, New York, 1971, Blakiston sion, McGraw-Hill Book Company, p. 533.
1
of clinical B. Saunders
/ I
0.: Clinical immunology, New & Row, Publishers, p. 352.
1
in Divi-
1 I I
see Szentivanyi, A.: The beta adrenergic theory of the atopic abnormality in bronchial asthma, J. Allergy, 42: 203-232, 1968.
i 1 I