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Antimicrobial Agents and Chemotherapy, November 2000, p. 3232-3234, Vol. 44, No. 11
0066-4804/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Updated Sequence Information and Proposed Nomenclature for blaTEM Genes and Their Promoters

V. Leflon-Guibout, B. Heym, and M.-H. Nicolas-Chanoine*

Microbiology Department, Hôpital Ambroise-Paré, Université Paris V, 92100 Boulogne-Billancourt, France

Received 23 February 2000/Returned for modification 29 June 2000/Accepted 16 August 2000


    ABSTRACT
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The nucleotide sequences of 59 blaTEM genes encoding inhibitor-resistant TEM enzymes showed great genetic variability and were associated with different types of promoters. These findings led us to suggest an updated blaTEM gene nomenclature based on the origin of the blaTEM gene (blaTEM-1A, blaTEM-1B, blaTEM-1C, blaTEM-1D, blaTEM-1E, and blaTEM-1F) and the promoter type.


    TEXT
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An updated blaTEM gene nomenclature was recently proposed by Goussard and Courvalin on the basis of the sequences of structural blaTEM genes and their promoters then available (8). Thus, blaTEM-1C was differentiated from blaTEM-1A and blaTEM-1B, and subgroups were defined and designated a, b, and c for a given blaTEM gene derivative, such as blaTEM-33a, blaTEM-33b, and blaTEM-33c, because of their relation to a certain number of nucleotide differences in their structural gene sequence. Upon first reading, this designation could be thought to be related to the fact that the genes are derived from blaTEM-1A, blaTEM-1B, or blaTEM-1C. However, upon closer reading, one can observe that it is sometimes related to the gene origin and at other times to the chronological appearance of the gene in the literature. Moreover, derivatives were also distinguished from each other by the type of their promoters, namely, the weak promoter P3 (C32 and G162) and the two strong overlapping promoters Pa and Pb (C32T and G162), and P4 (C32 and G162T), but this distinction was apparently not included in the gene designation (8).

In a recent multicenter study, which we performed to assess the evolution of amoxicillin-clavulanate resistance in Escherichia coli, the single-strand conformation polymorphism-PCR method was used to screen the blaTEM genes which differed from the reference blaTEM-1A, blaTEM-1B, and blaTEM-2 genes (9). Sequencing performed as previously described (11) on these blaTEM derivatives and their promoters allowed us to identify new genetic features of blaTEM genes. We found blaTEM-1B genes with the two different strong promoters (Pa and Pb, P4), and three new blaTEM genes, namely, blaTEM-1D, blaTEM-1E, and blaTEM-1F (9). In addition, among the 68 blaTEM genes which we have identified as encoding inhibitor-resistant TEM (IRT) enzymes, 9 encoded new enzymes and 59 encoded previously described enzymes (9). This article focuses specifically on the nucleotide sequences of these 59 IRT-encoding genes whose great genetic variability, which is shown in Table 1, justifies a new nomenclature of blaTEM genes based on the origin of the gene (i.e., blaTEM-1A, blaTEM-1B, blaTEM-1C, blaTEM-1D, blaTEM-1E, or blaTEM-1F) and the type of promoter.

                              
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  		TABLE 1.   Nucleotide mutations and amino acid substitutions in IRT beta -lactamase-encoding genes compared with blaTEM-1A, blaTEM-1B, blaTEM-1C, blaTEM-1D, blaTEM-1E, blaTEM-1F, and blaTEM-2 genes

Among the 17 blaTEM-30 genes of this study, seven groups could be defined by taking into account the blaTEM gene from which they were derived and their promoter type. One gene (strain 701055) was derived from blaTEM-1A and possessed the P3 promoter, whereas two others (representative strain 813014), which also originated from blaTEM-1A possessed the Pa and Pb promoters. Subsequently, we suggest that these genes be designated blaTEM-30a (P3) and blaTEM-30a (Pa/Pb), respectively. Another blaTEM-30 gene (strain 614131) was derived from blaTEM-1D but had the strong Pa and Pb promoters instead of the weak P3 promoter. We suggest designating this gene blaTEM-30d (Pa/Pb). Six other blaTEM-30 genes (representative strain 610087) were derived from blaTEM-1F and could be called blaTEM-30f (P4). The seven remaining blaTEM-30 genes all came from blaTEM-1B, but three of these genes (representative strain 803170) had promoter P3, three others (representative strain 806162) had promoters Pa and Pb, and one (strain 811006) had promoter P4. We suggest calling these genes blaTEM-30b (P3), blaTEM-30b (Pa/Pb), and blaTEM-30b (P4), respectively.

The three blaTEM-34 genes displayed three different nucleotide sequences. The first one (strain 609012) was derived from blaTEM-1A with promoters Pa and Pb and could be called blaTEM-34a (Pa/Pb), whereas the second one (strain 811069) was derived from blaTEM-1B and also had promoters Pa and Pb and could subsequently be called blaTEM-34b (Pa/Pb). The third one (strain 702065) was derived from blaTEM-1F and could be called blaTEM-34f (P4).

The same principle of nomenclature was applied to the other blaTEM genes (blaTEM-33, blaTEM-35, blaTEM-36, blaTEM-37, blaTEM-38, blaTEM-39, and blaTEM-40) as indicated in Table 1.

When we compared the nucleotide sequences of all these genes to those of the corresponding previously described genes, we found that in some cases the previously published genes corresponded to blaTEM-30b (Pa/Pb), blaTEM-30f (P4), blaTEM-34f (P4), blaTEM-35f (P4), and blaTEM-36f (P4) (6, 11). Only one specimen was identified in our study for blaTEM-31, blaTEM-33, and blaTEM-38 genes. The nucleotide sequence of our blaTEM-31 gene was different from the one which had already been published but without its promoter sequence. However, both genes are derived from blaTEM genes that have not been identified yet (2). Consequently, only the promoter type was specified in the designation of our blaTEM-31 gene (Table 1).

As indicated in Table 2, the blaTEM-33 gene identified in this study differs from the three previously published genes (8, 11). According to the blaTEM nomenclature we have now suggested, the blaTEM-33 genes that Goussard et al. called blaTEM-33a, blaTEM-33b, and blaTEM-33c are renamed blaTEM-33 (P3), blaTEM-33b (Pa/Pb) and blaTEM-33f (P4), because the first one was derived from a blaTEM gene that has not been named yet, the second one was derived from blaTEM-1B, and the third one was derived from blaTEM-1F.

                              
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  		TABLE 2.   Nucleotide mutations and amino acid substitutions in four blaTEM-33 genes compared with blaTEM-1A, blaTEM-1B, blaTEM-1C, blaTEM-1D, blaTEM-1E, blaTEM-1F, and blaTEM-2 genes

In conclusion, the analysis of a large number of blaTEM genes led us to suggest an updated nomenclature of blaTEM genes. Thus, we think that designating a given blaTEM derivative with a number and suffix corresponding to the original blaTEM gene (1A, 1B, 1C, 1D, 1E, and 1F) and its promoter is more comprehensible than using the suffix a, b, or c, etc., in relation to their chronological appearance in the literature, which does not permit any deduction of the original blaTEM nucleotide sequence. In cases where the original gene has not yet been identified, we suggest that the suffix be omitted (for example, blaTEM-33 [P3]). Moreover, this study confirms what has previously been observed on a sporadic basis, namely, that IRT-encoding genes display strong promoters very frequently (51 of 59 in this study) (3-6, 9-11).


    ACKNOWLEDGMENTS

We thank R. Labia for helpful discussions.

We are grateful to Hoechst Marion Roussel for financial support of this study.


    FOOTNOTES

* Corresponding author. Mailing address: Microbiology Department, Hôpital Ambroise-Paré, Université Paris V, 9 avenue Charles de Gaulle, 92100 Boulogne-Billancourt, France. Phone: 33 1 49 09 55 40. Fax: 33 1 49 09 59 21. E-mail: marie-helene.nicolas-chanoine{at}apr.ap-hop-paris.fr.


    REFERENCES
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1. Ambler, R. P. 1980. The structure of beta -lactamases. Philos. Trans. R. Soc. Lond. B 289:321-331[Abstract/Free Full Text].
2. Belaaouaj, A., C. Lapoumeroulie, M. M. Caniça, G. Vedel, P. Névot, R. Krishnamoorthy, and G. Paul. 1994. Nucleotide sequences of the genes coding for the TEM-like beta -lactamases IRT-1 and IRT-2 (formerly called TRI-1 and TRI-2). FEMS Microbiol. Lett. 120:75-80[Medline].
3. Bermudes, H., F. Jude, E. B. Chaibi, C. Arpin, C. Bebear, R. Labia, and C. Quentin. 1999. Molecular characterization of TEM-59 (IRT-17), a novel inhibitor-resistant TEM-derived beta -lactamase in a clinical isolate of Klebsiella oxytoca. Antimicrob. Agents Chemother. 43:1657-1661[Abstract/Free Full Text].
4. Bret, L., C. Chanal, D. Sirot, R. Labia, and J. Sirot. 1996. Characterization of an inhibitor-resistant enzyme IRT-2 derived from TEM-2 beta -lactamase produced by Proteus mirabilis strains. J. Antimicrob. Chemother. 38:183-191[Abstract/Free Full Text].
5. Caniça, M. M., M. Barthelemy, L. Gilly, R. Labia, R. Krishnamoorthy, and G. Paul. 1997. Properties of IRT-14 (TEM-45), a newly characterized mutant of TEM-type beta-lactamases. Antimicrob. Agents Chemother. 41:374-378[Abstract].
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11. Speldooren, V., B. Heym, R. Labia, and M.-H. Nicolas-Chanoine. 1998. Discriminatory detection of inhibitor-resistant beta -lactamases in Escherichia coli by single-strand conformation polymorphism-PCR. Antimicrob. Agents Chemother. 42:879-884[Abstract/Free Full Text].
12. Sutcliffe, J. G. 1978. Nucleotide sequence of the ampicillin resistance gene of Escherichia coli plasmid pBR322. Proc. Natl. Acad. Sci. USA 75:3737-3741[Abstract/Free Full Text].

Antimicrobial Agents and Chemotherapy, November 2000, p. 3232-3234, Vol. 44, No. 11
0066-4804/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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