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Vol. 95, pp. 65786583, June 1998
Perspective
Prokaryotes: The unseen majority
William B. Whitman*, David C. Coleman, and William J. Wiebe
Departments of *Microbiology, Ecology, and Marine Sciences, University of Georgia, Athens GA 30602
ABSTRACT
The number of prokaryotes and the total
amount of their cellular carbon on earth are estimated to be
46 3 1030 cells and 350550 Pg of C (1 Pg 5 1015 g),
respectively. Thus, the total amount of prokaryotic carbon is
60100% of the estimated total carbon in plants, and inclusion
of prokaryotic carbon in global models will almost double
estimates of the amount of carbon stored in living organisms.
In addition, the earths prokaryotes contain 85130 Pg of N
and 914 Pg of P, or about 10-fold more of these nutrients than
do plants, and represent the largest pool of these nutrients in
living organisms. Most of the earths prokaryotes occur in the
open ocean, in soil, and in oceanic and terrestrial subsurfaces,
where the numbers of cells are 1.2 3 1029, 2.6 3 1029, 3.5 3
1030, and 0.252.5 3 1030, respectively. The numbers of heterotrophic prokaryotes in the upper 200 m of the open ocean,
the ocean below 200 m, and soil are consistent with average
turnover times of 625 days, 0.8 yr, and 2.5 yr, respectively.
Although subject to a great deal of uncertainty, the estimate
for the average turnover time of prokaryotes in the subsurface
is on the order of 12 3 103 yr. The cellular production rate
for all prokaryotes on earth is estimated at 1.7 3 1030 cellsyyr
and is highest in the open ocean. The large population size and
rapid growth of prokaryotes provides an enormous capacity
for genetic diversity.
Although invisible to the naked eye, prokaryotes are an
essential component of the earths biota. They catalyze unique
and indispensable transformations in the biogeochemical cycles of the biosphere, produce important components of the
earths atmosphere, and represent a large portion of lifes
genetic diversity. Although the abundance of prokaryotes has
been estimated indirectly (1, 2), the actual number of prokaryotes and the total amount of their cellular carbon on earth
have never been directly assessed. Presumably, prokaryotes
very ubiquity has discouraged investigators, because an estimation of the number of prokaryotes would seem to require
endless cataloging of numerous habitats.
To estimate the number and total carbon of prokaryotes on
earth, several representative habitats were first examined. This
analysis indicated that most of the prokaryotes reside in three
large habitats: seawater, soil, and the sedimentysoil subsurface. Although many other habitats contain dense populations,
their numerical contribution to the total number of prokaryotes is small. Thus, evaluating the total number and total
carbon of prokaryotes on earth becomes a solvable problem.
Aquatic Environments. Numerous estimates of cell density,
volume, and carbon indicate that prokaryotes are ubiquitous in
marine and fresh water (e.g., 35). Although a large range of
cellular densities has been reported (104107 cellsyml), the
mean values for different aquatic habitats are surprisingly
similar. For the continental shelf and the upper 200 m of the
open ocean, the cellular density is about 5 3 105 cellsyml. A
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6578
Habitat
Marine
Continental shelf
Open ocean
Water, upper 200 m
Water, below 200 m
Sediment, 010 cm
Fresh
Lakes
Rivers
Saline lakes
Total
Volume,*
cm3
Cellsyml,
3 105
2.03 3 1020
7.2 3 1022
1.3 3 1024
3.6 3 1019
5
0.5
4600
1.25 3 1020
1.2 3 1018
1.04 3 1020
10
10
10
Total no.
of cells,
3 1026
1.0
360
650
170
1.3
0.012
1.0
1180
Ecosystem type*
Area,
3 1012 m2
No. of cells,
3 1027
17.0
7.5
5.0
7.0
12.0
8.0
15.0
9.0
18.0
14.0
8.0
2.0
123.0
1.0
0.5
0.3
0.4
0.6
28.1
52.7
31.6
63.2
49.1
20.8
7.3
255.6
6579
Cellsycm3,
3 106
Deep
oceans
220.0
66.0
45.0
121.5
6.2
18.6
19.0
57.0
4.0
12.0
7.8
0.95i
0.61i
0.44i
0.34i
Total
275.1
Grand Total: 380 3 1028 5 3.8 3 1030
0.1
10
100
200
300
400
600
1,200
2,000
3,000
Continental shelf
and slope
Coastal
plains
14.5
26.6
4.1
12.5
2.6
10.1
3.7
3.2
2.6
4.4
8.1
1.2
3.8
0.8
3.2
1.2
1.0
0.9
0.7
25.3
79.9
6580
Animal
Human
Cattle
Sheep and goats
Pigs
Domestic birds
Termites
Organ
Colon
Rumen
Rumen
Colon
Cecum
Cecum
Hindgut
Cellsyml or
cellsyg
1011
3.2 3
2.1 3 1010
4.4 3 1010
5.4 3 1010
2.8 3 1010
9.5 3 1010
2.7 3 106
Organ
contents*
220
106
12
9
1
2
g
liter
liter
liter
liter
g
No. of
animals
109
5.6 3
1.3 3 109
1.7 3 109
8.8 3 108
8.8 3 108
1.3 3 1010
2.4 3 1017
No. of cells,
3 1023
Refs.
3.9
29.0
9.0
4.3
0.3
0.024
6.5
45, 46
47, 48
47, 48
49, 50
49, 50
51, 52
53
*Organ contents in volume or grams of wet weight. For comparison, the volume of the human colon is 0.5 liter. For domestic
birds, weight wet was calculated from a volume of 2 ml assuming that 1 ml - 1 g wet weight.
Values from the FAO Production Yearbook (54), except for the termites value which was from ref. 55.
The direct count was assumed to be 2.7 3 viable count (56).
Includes chickens, ducks, and turkeys.
Per termite.
Environment
No. of
prokaryotic cells,
3 1028
Pg of C in
prokaryotes*
Aquatic habitats
Oceanic subsurface
Soil
Terrestrial subsurface
Total
12
355
26
25250
415640
2.2
303
26
22215
353546
Ecosystem
Net primary
productivity,*
Pg of Cyyr
Plant*
Subsurface
prokaryotes
Terrestrial
Marine
48
51
560
1.8
26
2.2
22215
303
6581
Population
size
Turnover time,
days
Cellsyyr,
3 1029
3.6 3 1028
28
8.2 3 10
2.9 3 1027
2.6 3 1029
4.9 3 1030*
4.3 3 1024
16*
300*
1.5
900*
5.5 3 105*
1
8.2
1.1
7.1
1.0
0.03
0.02
6582
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
90.
91.
6583
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