Estimating prokaryotic diversity and its limits.
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Journal: 2002/September - Proceedings of the National Academy of Sciences of the United States of America
ISSN: 0027-8424
Abstract:
The absolute diversity of prokaryotes is widely held to be unknown and unknowable at any scale in any environment. However, it is not necessary to count every species in a community to estimate the number of different taxa therein. It is sufficient to estimate the area under the species abundance curve for that environment. Log-normal species abundance curves are thought to characterize communities, such as bacteria, which exhibit highly dynamic and random growth. Thus, we are able to show that the diversity of prokaryotic communities may be related to the ratio of two measurable variables: the total number of individuals in the community and the abundance of the most abundant members of that community. We assume that either the least abundant species has an abundance of 1 or Preston's canonical hypothesis is valid. Consequently, we can estimate the bacterial diversity on a small scale (oceans 160 per ml; soil 6,400-38,000 per g; sewage works 70 per ml). We are also able to speculate about diversity at a larger scale, thus the entire bacterial diversity of the sea may be unlikely to exceed 2 x 10(6), while a ton of soil could contain 4 x 10(6) different taxa. These are preliminary estimates that may change as we gain a greater understanding of the nature of prokaryotic species abundance curves. Nevertheless, it is evident that local and global prokaryotic diversity can be understood through species abundance curves and purely experimental approaches to solving this conundrum will be fruitless.
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Proc Natl Acad Sci U S A 99(16): 10494-10499
PMID: 12097644

Estimating prokaryotic diversity and its limits

Department of Civil Engineering, Centre for Molecular Ecology, and Neural Systems Group, Department of Psychology, University of Newcastle upon Tyne, Newcastle upon Tyne NE1 7RU, United Kingdom; and Department of Civil Engineering, University of Glasgow, Glasgow GL12 8LT, United Kingdom
To whom reprint requests should be addressed. E-mail: ku.ca.lcn@sitruc.mot.
Edited by Robert May, University of Oxford, Oxford, United Kingdom, and approved May 22, 2002
Edited by Robert May, University of Oxford, Oxford, United Kingdom, and approved May 22, 2002
Received 2001 Dec 18
Copyright © 2002, The National Academy of Sciences

Abstract

The absolute diversity of prokaryotes is widely held to be unknown and unknowable at any scale in any environment. However, it is not necessary to count every species in a community to estimate the number of different taxa therein. It is sufficient to estimate the area under the species abundance curve for that environment. Log-normal species abundance curves are thought to characterize communities, such as bacteria, which exhibit highly dynamic and random growth. Thus, we are able to show that the diversity of prokaryotic communities may be related to the ratio of two measurable variables: the total number of individuals in the community and the abundance of the most abundant members of that community. We assume that either the least abundant species has an abundance of 1 or Preston's canonical hypothesis is valid. Consequently, we can estimate the bacterial diversity on a small scale (oceans 160 per ml; soil 6,400–38,000 per g; sewage works 70 per ml). We are also able to speculate about diversity at a larger scale, thus the entire bacterial diversity of the sea may be unlikely to exceed 2 × 10, while a ton of soil could contain 4 × 10 different taxa. These are preliminary estimates that may change as we gain a greater understanding of the nature of prokaryotic species abundance curves. Nevertheless, it is evident that local and global prokaryotic diversity can be understood through species abundance curves and purely experimental approaches to solving this conundrum will be fruitless.

Abstract

The ability to measure bacterial diversity is a prerequisite for the systematic study of bacterial biogeography and community assembly. It is therefore central to the ecology of surface waters, the oceans and soils, waste treatment, agriculture, and global elemental cycles. However, the experimental definition of bacterial diversity has never been undertaken for any naturally occurring bacterial community anywhere, and the extent of prokaryotic diversity is widely held to be beyond practical calculation (1).

Our understanding of bacterial biogeography and community assembly is correspondingly vague, anecdotal, and controversial. For example, the global distribution of some aquatic protozoa has been used to assert that the entire microbial world is composed of a small number of ubiquitous organisms (2, 3), whereas the apparently endemic distribution of some bacteria has been used to suggest the opposite (4, 5). Perhaps more importantly, the inability to estimate diversity inhibits microbial ecologists from using or testing established theories of biogeography and community assembly, even though the complex nature of the microbial world means that microbial ecology is severely constrained by a lack of theory.

However, to estimate the extent of microbial diversity, it is not necessary to count every single species or taxa in a sample. It is sufficient to simply estimate the area under the bacterial species abundance curve for that environment. There is insufficient experimental evidence to support a particular parametric description of this curve. However, MacArthur (6) and later May (7) deduced that the highly dynamic and random growth that is thought to be characteristic of prokaryotes would lead to a lognormal species abundance curve. Subsequent work by statistical mathematicians, also assuming random growth, has confirmed this finding in exponential and logistic growth scenarios (8, 9).

On this basis, we are able to show how relatively easy to measure variables can be used to define bacterial diversity. The work does not presuppose a particular definition of a species, merely the existence of credible criteria for distinguishing between different organisms. For the purpose of this paper, this means a meaningful difference in the sequence of the 16S RNA gene. We use the term taxa as a shorthand for groups of bacteria that can be distinguished on that basis.

Acknowledgments

We thank Ian Head, Robert May, Dan Dykhuizen, Rudi Amman, E. O. Wilson, and Ian Thompson for much-needed encouragement.

Acknowledgments

Abbreviations

  • FISH, fluorescent in situ hybridization

  • AOB, ammonia oxidizing bacteria

Abbreviations

Notes

This paper was submitted directly (Track II) to the PNAS office.

See commentary on page 10234.

Notes
This paper was submitted directly (Track II) to the PNAS office.
See commentary on page 10234.

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