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The Andersen-Everett reclassification

Editorial comment

[The following is the text of a presentation on chlamydial taxonomy by Dr. Karin Everett, presented orally at the Fourth meeting of the European Society for Chlamydia research Helsinki, Finland, August 2000, and still very relevant. This site has added some additional references and access to a web-based resource, and a further document follows after this topic].

Everett et al‘s reclassification was an emotional issue for many chlamydiologists. An impressive number of eminent chlamydiologists, most not taxonomists, were vehemently opposed to the reclassification. Their objections were summarised in a letter [Schachter et al., 2001] to the International Journal of Systematic and Evolutionary Microbiology (IJSEM) to which the authors of the ‘new’ classification replied [Everett & Andersen, 2001].

While the presence of 9 species within the Chlamydiaceae was not particularly controversial, the main criticisms were that:

  • there is insufficient reason to divide the former Chlamydiaceae into 2 new genera and that this is counterintuitive
  • it had taken a long time to get clinicians used to Chlamydia and would be confusing for them. Doesn’t this underestimate our clinical colleagues?
  • there is too much emphasis on limited nucleotide sequence data and insufficient consideration of basic biological characteristics. This is inevitable given the objectivity of sequence data and the variability intrinsic in biological characteristics.
  • the evidence for some species and families, notably the Waddliaceae and the Simkaniaceae, rests on limited data derived from a single isolate. This is less true now.
  • some objected to the genus name Chlamydophila which literally means “like Chlamydia”.This name doesn’t exactly trip off the tongue but blames the taxonomy authorities [Storz and Page] for that.
    New taxonomies are never ideal and very often controversial. It is human to resist change, human to regret one didn’t get round to it oneself. Quite correctly, Everett et al consulted ‘leading’ chlamydial labs widely prior to publication of their reclassification. Some of the replies which I saw, from persons I would otherwise respect, were intemperate at least. On scientific grounds, there can be no doubt that the reclassification was vastly superior to the old classification because it incorporated more recent molecular knowledge and views on microbial evolution. This writer publicly declined to sign the widely circulated objection letter, a decision which, years later, I view as correct at that time. The resulting sharp exchange of emails was wittily and with reason named by one chlamydial ‘wag’ the “taxon wars”. My view was, and remains, that the reclassification, having been duly reviewed and approved by leading taxonomic authorities outside chlamydiae, should prevail until superseded by newer knowledge or a more rational system. Stephens (2008) has cogently argued that the genus Chlamydophila in the family Chlamydiaceae should be abandoned. This proposal has been accepted by Bergey but only preliminary details have yet emerged. Proponents of this LatestClassification are invited to complete this wiki word stub and to present their case.Meanwhile, the Everett et al reclassification, despite all objections, is being widely used, particularly by the upcoming generation of researchers. Indeed, citation research indicates that the Everett et al classification paper is far the most widely quoted of all modern chlamydial research papers!Taxonomies are not immutably scribed on tablets of stone, though, in 2008, chlamydial taxonomy is at something of a crossroads Taxonomy supplement, mainly due to changes in the rules which are difficult to meet with chlamydiae. This site is pleased to encourage and publish scientific comments relating to the taxonomy and extraordinary diversity of the Chlamydiales and alternative views are very welcome.[MEW] August 2010]

Taksonomia: the science of describing, identifying, naming, and classifying organisms

Karin Everett, Department of Medical Microbiology and Parasitology, University of Georgia, Athens, Georgia, USA.

265 years ago a 28-year-old Swedish medical student needed a workable system to identify the huge number of plants and animals that were being brought back to Europe from Asia, Africa, and the Americas. So he invented binomial taxonomic naming, giving each organism a two-word Latin name. This system was so useful that the medical student, Carolus Linnaeus, has been called the father of modern taxonomy.

Linnaeus’ two books still contain the oldest plant and animal names that are accepted as valid today. His naming method is systematic, functional and predictive. Linnaeus and the taxonomists who followed him knew that organisms from undescribed taxa could not be identified. Thus, when bacteria began to be identified, they too were named using Linnaeus’ method. The result of taxonomy for microbiologists is the identification/diagnostic process.

Modern microbiology began in 1923 with the publication of the 1st edition of Bergey’s Manual of Determinative Bacteriology. These were busy years for microbiology and taxonomy.

For taxonomists, the formation of the Commission on Naming & Taxonomy was especially important, because it led to the publication of the Bacteriological Code the year after I was born. The code contains all the rules and recommendations for using bacterial names.

And of course, they led to the creation of The Bulletin, which was later named the I.J.S.B. and then I.J.S.E.M. It was published in my hometown, Ames, Iowa by the American Society for Microbiology, then republished in Maryland. This has been the voice of the Bacteriological Code for 50 years. Incidentally, Ames is also where Arthur Andersen, who coauthored the reclassification of chlamydiae, took his veterinary degree. This is also where Les Page lived and worked.

Between 1945 and 1971 there were 10 attempts to classify chlamydiae into orders, families, tribes, sub tribes, genera, and species, see Chlamydiales History. The Page classification was ultimately successful, while the others were not. Why?

First, it was systematic, based only on stable phenotypic traits. It was useful, as evidenced by a quarter century of publications. And it was predictive. For example:

According to the Bacteriological Code, a bacterium can be named only by being published in the International Journal of Systematic Bacteriology (IJSB) (now the International Journal of Systematic and Evolutionary Microbiology, IJSEM). Dr. Page was the head of the committee assigned by the American Society of Microbiology (ASM), the publisher of IJSB, to handle chlamydial taxonomy.

The ASM classification of bacteria was based on numerical taxonomy, which uses only plus/minus data. Consistent with the ASM approach, Page limited Chlamydiaceae to two species and based them on “relatively stable morphological and chemical characteristics rather than on their presumed host or tissue preferences or on the specific serology of their cell wall antigens.”

Numerical taxonomy had been used for bacteria since 1956. Looking back through IJSB from these years, you will find long numerical matrices correlating hundreds of phenotypic characters into similarity clusters for many bacteria. Numerical criteria were considerably more stringent than previous taxonomic criteria.

“Only characters that were a direct or indirect result of the genotype of the organism” could be employed. These included morphology, biochemistry, culture characteristics, physiology, nutritional requirements, antigenic composition, and phage sensitivity. Consequently, when IJSB published the Approved Lists of Bacteria in 1980, Page’s two species, C. trachomatis, and C. psittaci were retained although 90% of all bacterial names were discarded at that time. These days, the approved list of names is on the web.

In the following years, there were no changes to chlamydial taxa because large quantities of plus/minus data were not available.

This began to change in 1988. DNA-DNA reassociation had been accepted since 1981 as a fundamental method for distinguishing both genera and species. In 1988, Rachel Cox and colleagues at the University of Washington showed that DNA-DNA reassociation could be used to distinguish chlamydial strains. In the following year, Fukushi and Hirai expanded on the analysis.

Cox’s and Fukushi’s data suggested that there were perhaps 8 species and 4 genera in the Chlamydiaceae, using criteria that are still accepted today. Their proposals of C. pneumoniae and C. pecorum were consistent with their data. The end result was useful and predictive for some groups, but not for others. Because they were not based on uniformly applied taxonomic principles, the resulting 4-species taxonomy violated the central taxonomic principles of systematic construction, stable traits, functionality and predictive ability:

Furthermore, logical provisions were absent for handling new taxa.

Today, taxonomic decision making is based on numerical and evolutionary criteria.

So what is the process for correcting such a situation? The first step for us was the accumulation of new information, primarily ribosomal sequence data. When the implications of the data became evident, we consulted with as many chlamydiologists as we could, asking for suggestions and providing prepublication data to people in more than 30 labs. Then Art, Robin, and I went over it all using present-day methods and criteria:

We used primarily three types of data. It included a table of DNA-DNA reassociation data from the 1980’s and early ‘90’s, a table of ecological data, several qquartetspuzzling phylogenetic trees depicting evolutionary relationships in six genetic loci. These allowed us to infer the evolutionary structure of the Order Chlamydiales. Because evolutionary inference was included in taxonomic decision-making, construction of the classification has become a scientific exercise and so produced a testable hypothesis.

The hypothesis produced by ribosomal sequence analyses was the divergence of the genera Chlamydia and Chlamydophila. We have now tested this by analyzing 5 coding genes. Bjorn Herrmann and Bertil Pettersson have tested it using rnpB. The separation of the genera passed these tests with flying colors. This hypothesis of separated genera can also be tested by analysis of other genes or by comparisons of genome structure. An approach we would recommend for generating new hypotheses about evolutionary relationships is the genomic analysis of other families in the Chlamydiales. Currently microbiologists have pretty clear criteria for recognizing species and genera.

Genera are also based on reassociation and clustering, with the added feature that the 16S sequences of closely related bacterial genera tend to be about 95% identical.

Criteria for higher taxa are less well resolved:

For the time being, all members of the Order Chlamydiales have an obligate intracellular lifestyle and developmental cycle, and all have at least 80% 16S or 23S ribosomal sequence identity . The current 4 families are quite distinct. The Chlamydiaceae is the only family that can be detected with antibodies to the group-specific LPS, and its species have at least 90% ribosomal sequence identity. By all measures, the G+C content of Chlamydiaceae spp. is about 40 mol%.

The Bacteriological Code no longer operates independently of the Codes for Zoological or Botanical Nomenclature. In concert with this change and a more inclusive mission, IJSB has become IJSEM. It is now published by the Society for General Microbiology in the UK. To be valid, new names and combinations must be acceptable within the context of all three Codes and so must be approved by Hans Truper at IJSEM and published or listed in IJSEM. Not all of the names Art and I initially wanted to propose for chlamydiae were acceptable. For example, the genus name Chlamydophila, which appears in the approved list of bacterial names, was eventually chosen by Hans Truper and Johannes Storz working together.

There is no provision for rescinding a validly published name. A validly published name never dies. Names are used at the discretion of authors and scientists, who are expected to decide for themselves which correct name to use. Their choices must be consistent with the circumscription they are using. For example, if a Family has two validly published genera, according to one study, and four according to another, as an author you may follow only one of these approaches in your manuscript. In this way, it is possible for two or more validly published names to remain in use.

Does taxonomy have policemen? No.

Neither IJSEM nor the Code acts or prevents authors from using either valid or invalid names in publication. That responsibility resides with authors and reviewers. The name Bedsonia, for example, is an illegitimate name for Chlamydiathat was proposed in 1953, has been widely used and has appeared in publications as recently as 1984.

Changes in taxonomy take place because we acquire new information. Systematists agree that phenotypic, genetic, and phylogenetic analyses should be combined, in so far as possible, as a basis for taxonomy. The unification of these powerful methods is revolutionizing taxonomy in general and chlamydial taxonomy specifically, providing coherent clusters of ecologically and genetically similar bacteria.

Our 1999 reclassification of bacteria in the order Chlamydiales is systematic, depends on measurable traits, and is predictive on several taxonomic levels. It provides descriptive tools for newly discovered chlamydiae. It provides descriptions and names so that taxa can be identified. I believe that insights gained from relationships among these taxa will eventually allow us to predict the pathology of these species.

Acknowledgement. The final slide is derived by KDE from: Horn M., Wagner M., Muller KD., Schmid EN., Fritsche TR., Schleifer KH., Michel R. Neochlamydia hartmannellae gen. nov., sp. nov. (Parachlamydiaceae), an endoparasite of the amoeba Hartmannella vermiformis. Microbiology UK, 146, 1231-9 (2000).

[KDE] August 2000

[MEW comment: Use of the Everett Andersen taxonomy has increased in the literature as researchers become aware of it. It is being used by key organizations like the American Type Culture Collection, the NCBI taxonomy browser and the Sanger Institute genome databases among others. TIGR (now Craig-Ventner Inst) sticks to Chlamydia pneumoniae AR39 while acknowledging under taxonomy the genus name Chlamydophila!

There is an issue here as to whether prestigious scientific institutions should take a leading role in introducing approved taxonomies, or wait until everyone is aware of them. The split of the Chlamydiaceae into two genera has proved unpopular with many chlamydiologists, leading to the even newer Stephens Horn Kuo classification which has been validated by Bergey’s manual. Members of the community are invited to create a page for this latest classification (having first registered) by double-clicking on the unfulfilled WikiWord: StephensHornKuo .]

NEXT: The Rules of Taxonomy and their effect on the classification of the Chlamydiales.


Bush, R. M. & Everett, K. D. E. (2001). Molecular evolution of the Chlamydiaceae. International Journal of Systematic and Evolutionary Microbiology 51, 203 – 220. Full paper [Acrobat]

Everett, K. D. E., Bush, R. M. & Andersen, A. A. (1999). An emended description of the order Chlamydiales, a proposal of Parachlamydiaceae fam. nov. and Simkaniaceae fam. nov., each containing one monotypic genus, revised taxonomy of the family Chlamydiaceae, including a new genus and five new species, and standards for the identification of organisms. International Journal of Systematic and Evolutionary Bacteriology 49, 415 – 440. Full paper [Acrobat]

Everett, K. D. E. & Andersen, A. A. (2001). Radical changes to chlamydial taxonomy are not necessary just yet – reply. International Journal of Systematic and Evolutionary Microbiology 51, 250. Full letter [Acrobat]

Everett, K. D. E. & Andersen, A. A. (1999). Identification of nine species of the Chlamydiaceae using PCR-RFLP. _International Journal of Systematic Bacteriology 49, 803 – 813. Full paper [Acrobat]

Everett, K. D. E. & Andersen, A. A. (1997). The ribosomal intergenic spacer and domain I of the 23S rRNA gene are phylogenetic markers for Chlamydia spp. International Journal of Systematic Bacteriology 47, 461 – 473.

Kahane, S., Everett, K. D. E., Kimmel, N. & Friedman, M. G. (1999). Simkania negevensis strain Z(T): growth, antigenic and genome characteristics. International Journal of Systematic Bacteriology 49, 815 – 820.

Schachter, J., Stephens, R. S., Timms, P., Kuo, C., Bavoil, P. M., Birkelund, S., Boman, J., Caldwell, H., Campbell, L. A., Chernesky, M., Christiansen, G., Clarke, I. N., Gaydos, C., Grayston, J. T., Hackstadt, T., Hsia, R., Kaltenboeck, B., Leinonnen, M., Ojcius, D., McClarty, G., Orfila, J., Peeling, R., Puolakkainen, M., Quinn, T., Rank, R. G., Raulston, J., Ridgeway, G. L., Saikku, P., Stamm, W. E., Taylor-Robinson, D., Wang, S. P., Wyrick, P. B. (2001). Radical changes to chlamydial taxonomy are not necessary just yet (Letter) International Journal of Systematic and Evolutionary Microbiology 51, 249. Full letter [Acrobat] Authors reply [Acrobat]

Stephens, RS (2008). Divergence without a difference: phylogenetics and taxonomy resolved. In: Christiansen G (ed) Proceedings of the 6th meeting of the European Society for Chlamydia research, pp 131 – 136. Published by the University of Aarhus. ISBN:978-87-984259-3-9