Molecular Biology and Evolution 17:352-361 (2000)
© 2000 Society for Molecular Biology and Evolution
Articles |
Horizontal Gene Transfer of Glycosyl Hydrolases of the Rumen Fungi
,Department of Biochemistry and Biotechnology, Rovira i Virgili University, Catalonia, Spain
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Abstract |
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By combining analyses of G+C content and patterns of codon usage and constructing phylogenetic trees, we describe the gene transfer of an endoglucanase (celA) from the rumen bacteria Fibrobacter succinogenes to the rumen fungi Orpinomyces joyonii. The strong similarity between different glycosyl hydrolases of rumen fungi and bacteria suggests that most, if not all, of the glycosyl hydrolases of rumen fungi that play an important role in the degradation of cellulose and other plant polysaccharides were acquired by horizontal gene transfer events. This acquisition allows fungi to establish a habitat within a new environmental niche: the rumen of the herbivorous mammals for which cellulose and plant hemicellulose constitute the main raw nutritive substrate.
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Introduction |
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Lignocellulosic material is hard and difficult to digest. Terrestrial herbivores might be expected to have a set of enzymes that can digest the cellulose and other polysaccharide structures of plants. However, this is not so. Terrestrial animals have elaborated a different evolutive solution: symbiotic relationships with bacteria, protists, and fungi which carry out these activities in their own interests. The host provides heat, moisture, and food, while the microorganisms contribute protein as microbial biomass and by-products of digestion such as volatile fatty acids that the animal uses (Madigan, Martinko, and Parker 1997
). Anatomically, the most complex specialization is found among the ruminants, such as cattle or sheep, with elaborate, multicompartmentalized stomachs specialized for a herbivorous diet. The normal microbiota in this anoxic environment are composed of bacteria, ciliate and flagellate protozoa, and anaerobic chytridiomycete fungi (Flint 1997
; Gordon and Phillips 1998
). Because cellulose and plant hemicellulose are the most abundant carbon and energy source in the rumen, the glycosyl hydrolases (GHs) of these organisms must play a significant role in their homeostasis. In terms of molecular evolution, rumen is a complex ecosystem in which natural gene transfer and traffic of genetic material could well occur.
Rumen organisms produce a wide range of highly active GHs that work synergistically (Flint 1997
). So far, a number of genes and/or cDNAs which encode endoglucanases, exoglucanases, xylanases, lichenases, and mannanases have been cloned and sequenced from different species, including the anaerobic fungi Neocallimastix, Piromyces, and Orpinomyces. Most of the fungal GH sequences derived from these genes contain a dockerin-like reiterated sequence that mediates the assembly of a large multienzyme cellulosome-like complex (Fanutti et al. 1995
) which exhibits very high cellulase activity against crystalline cellulose (Wilson and Wood 1992
) and is similar to that described for Clostridium thermocellum (Beguin and Lemaire 1996
) and other bacteria (Karita, Sakka, and Ohmiya 1997
). The reiterated sequence conserved in rumen fungal cellulases differs from clostridial dockerins in size and amino acid sequence, and there is no detectable sequence similarity between them (Beguin and Lemaire 1996
).
No known GH gene from rumen fungi has any introns, and sequences of these genes are very similar to those of GH bacterial genes. On this basis, prokaryotic origins have been suggested for Neocallimastix frontalis celA (Fujino et al. 1998
), Neocallimastix patriciarum celB (Zhou et al. 1994
), xynA (Gilbert et al. 1992
) and xynB (Black et al. 1994
), Piromyces sp. manA (Fanutti et al. 1995
), and Orpinomyces sp. licA (Chen, Li, and Ljungdahl 1997
) and CelB (Chen et al. 1998
) genes and the noncatalytic domain of Orpinomyces joyonii celA (Liu et al. 1997
). However, these suggestions need a demonstration, and so, with this purpose in mind, we analyzed the G+C content, the codon usage, and the phylogenetic trees derived from the multialignment of orthologous sequences worked out so far for rumen fungi genes. For analytical comparisons, we used gene sequences from Fibrobacter succinogenes, a bacterium that also plays a predominant role in fiber digestion in the rumen (Matsui et al. 1998
).
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Materials and Methods |
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All available genes from rumen fungi and F. succinogenes strain S85 were imported from the EMBL database. To avoid distortions in the mean calculations of F. succinogenes, we did not include the sequences (EMBL codes L39838, L39839, X88561, L48039, and M58520) from other F. succinogenes strains that were homologous to some of the sequences from strain S85. Neither did we include the fragment of the CMC-xylanase gene from strain S85 (EMBL code U94826) with an anomalous G+C content. Table 1 shows a list of gene names, characteristics of the products (which include the glucoside hydrolase family, if any), EMBL accession numbers of the sequenced DNAs, and the numbers of base pairs for the coding regions.
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The cases of horizontal gene transfer were inferred by the method used previously (Garcia-Vallvé, Palau, and Romeu 1999
). In short, it is based on (1) G+C content, (2) codon usage analysis using a dendrogram derived from a Pearson linear correlation coefficient determined from a pairwise codon usage comparison, and (3) phylogenetic congruency testing. Because the codon usage patterns are species-specific, each gene in a genome tends to conform to the codon usage of its own species. This allows us to define the null hypothesis that GH-encoding genes of rumen fungi should cluster with the remaining fungal chromosomal genes and not form a distinct group.
As a measure of the distance between the codon usage of a gene (X) and the mean codon usage of an organism (
), we calculated the Hamming distance following a procedure similar to the one used for predicting protein structural classes (Chou and Zhang 1995
). Each gene therefore corresponds to a vector or a point in the 61-D space whose coordinates are the relative frequencies of use of the 61 codons. The stop codons are not included, and each organism corresponds to a vector or point whose coordinates are the mean values.
The Hamming distance is defined by:
where xi is the relative frequency of the ith codon for a gene and 
is the mean value for an organism. This method calculates a distance between the codon usage of a gene and the mean value for different organisms. The smallest distance corresponds to the organism whose codon usage is most similar to that of the gene considered.
The CAZy internet server (http://afmb.cnrs-mrs.fr/~pedro/CAZY/) was used to define the GH families (Henrissat and Bairoch 1996
). We imported the protein sequences and identified the catalytic domains from the information available in the SwissProt database or from local alignments against crystallized sequences. For xyn3 from N. frontalis, xynA from N. patriciarum, xynA from Piromyces sp., and xynC from F. succinogenes sequences with two GH family 11 catalytic domains, we used both domains. Multiple alignments, with final manual adjustments, and phylogenetic analysis were performed using the CLUSTAL W software package (Jeanmougin et al. 1998
). Bootstrap values were calculated in 1,000 replicates.
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Results |
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The mean value of the total G+C content of the 35 rumen genes was 39.9 ± 4.1%. The G+C contents (%) at the different codon positions were as follows: 49.3 ± 5.0 at first positions, 41.4 ± 4.2 at second positions, and 29.2 ± 8.4 at third positions. Applying the principle of G+C content analysis should also allow the detection of horizontal gene transfer. The individual G+C content at third codon positions showed a high value for the O. joyonii celA gene (56.9%), significantly higher than those for the other fungi genes and more similar to the third codon position G+C content of the bacteria F. succinogenes (mean value 62.6 ± 6.4). This already suggests a nonfungal source for the O. joyonii celA gene.
Figure 1 shows the codon usage analysis of the genes described in table 1 . We can see that (1) all of the F. succinogenes genes form a cluster, although the endB and tuf genes are somewhat separated; (2) the rumen fungi genes do not cluster on taxonomic grounds, but by joining related orthologous genes; (3) two subclusters of rumen fungi genes, which we have called GH of rumen fungi and non-GH of rumen fungi, respectively, are observed; (4) the O. joyonii celA gene cluster with the F. succinogenes group; and (5) the N. patriciarum xynB gene cluster separately.
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The different codon usage patterns between GH and non-GH genes of rumen fungi is surprising. The GH group includes several intronless GH genes of families 5, 6, 9, 10, 11, 16, and 26, three acetylxylan esterases (bnaI, bnaII, and bnaIII) from N. patriciarum that contain the dockerin domain sequence that binds to the cellulosome-like structure, and Orpinomyces sp. cyclophilin B (cypB). The non-GH group includes a malate dehydrogenase (mdh); aconitase (aco) and acetohydroxyacid reductoisomerase (adhr) from Piromyces sp., closely related to their mitochondrial homologs from aerobic eukaryotes (Akhmanova et al. 1998
), a hydrogenosomal malic enzyme (malic) from N. frontalis, very similar to malic enzymes from metazoa, plants, and protists (van der Giezen et al. 1997
); a putative enolase gene (E-1) from N. frontalis, interrupted by a large intron and with the canonical features of polyadenylation signal and intron-splicing boundaries of genes isolated from aerobic filamentous fungi (Durand et al. 1995
); a beta-succinyl-CoA synthetase (sucB) from N. frontalis, similar to fungi beta-succinyl-CoA synthetases; a phospho-enolpyruvate carboxikinase (ppcK) from N. frontalis; an acetylxylan esterase (axeA) from Orpinomyces sp. and a formate acetyltransferase (pf1); isocitrate dehydrogenase (idh); and hydrogenosomal adenylate kinase (hdg) from Piromyces sp.
The position of the N. patriciarum xynB gene, which clusters separately from other GH rumen fungi in figure 1
, can be explained by the highly biased amino acid content of the derived protein. This xylanase contains a noncatalytic 455-residue linker sequence comprising 57 repeats of an octapeptide rich in amino acids G, S, K, and N (Black et al. 1994
). When the relative synonymous codon usage (RSCU) values were used to construct this figure, the xynB gene clustered with the other GHs of rumen fungi (results not shown).
Table 2 shows the Hamming distance between the codon usage of the individual genes and the mean values of F. succinogenes and GH and non-GH rumen fungi groups defined in figure 1 . The shortest distance in all cases corresponds to the group that the gene belongs to. The O. joyonii celA gene has a Hamming distance of 0.31 with respect to the F. succinogenes mean value, while its distances from the GH and non-GH groups are much higher (0.73 and 0.62, respectively).
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To investigate the possible horizontal transfer of GH from rumen fungi, we aligned the catalytic domains of 54 endoglucanases of GH family 5 to a total length of 475 aa. The pairwise similarity between the sequences varies from 20.7 to 99.4, and the most conserved regions correspond to the scaffold ß-strands of a TIM barrel structure. Figure 2 shows the phylogenetic tree derived from the multialignment. Although some paralogous sequences exist, several features can be observed: (1) fungi and bacteria sequences cluster into two different branches, (2) the endoglucanases from rumen fungi are in the bacterial branch, (3) the bacterial sequence from the scotobacteria Burkholderia solanacearum clusters with the fungi branch, and (4) the Orpinomyces sp, celA sequence does not cluster with the other rumen fungi or any F. succinogenes endoglucanases. The multialignment of the catalytic domains of xylanases of GH family 11 consists of 64 sequences and a total length of 240 aa. The most conserved regions correspond to the ß-sheets of a ß-sandwich structure. Figure 3 shows the tree of this family, where rumen fungi xylanases are closely related to F. succinogenes, Ruminococcus albus, and Ruminococcus flavefaciens—three bacteria that also live in the rumen.
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Discussion |
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The acquisition of fresh genetic information is probably important for the vitality of a species (Krawiec and Riley 1990
). Bacterial speciation is therefore likely to be driven by a high rate of horizontal transfer (Martin 1999
), which introduces novel genes that permit the rapid exploitation of new environmental niches (Lawrence 1997
). Gene transfer between ruminal bacteria has been demonstrated in vitro (Morrison 1996
). The high microbial population density, i.e., 1010–1011 bacteria per milliliter of rumen fluid (Madigan, Martinko, and Parker 1997
), the bacteriophage population of the rumen (Swain, Nolan, and Klieve 1996
), and the existence of communities attached to substrate particles or the gut epithelium or inside the protozoal food vacuoles potentially favor gene transfer between a wide range of microorganisms within the rumen (Flint 1994
). Transfer of plasmids between strains of Escherichia coli under rumen conditions has therefore been demonstrated (Scott and Flint 1995
).
It is important to note the independent clustering of GH and non-GH, as seen in the dendrogram of Pearson correlation values (see fig. 1
). This can be correlated with a different expression of GH genes as compared with the other genes of rumen fungi (Sharp, Tuohy, and Mosurski 1986
). Since 15 codons (GCG, GAG, GGG, TTG, CTG, CTA, CCT, CCC, CCG, CAG, CGA, AGG, TCG, GTA, and TGA) are not used, the codon usage of the non-GH group is rather biased. This is a general feature of highly expressed genes. In addition, several eukaryotic homologs of genes in this group are highly expressed. This is the case for some genes involved in hydrogenosome function (including the malic enzyme) and the beta succinyl CoA synthetase gene in Trichomonas vaginalis (McInerney 1997
), and for the enolase gene in Saccharomyces cerevisiae (Sharp and Cowe 1991
). In this context, the GH group of genes is expressed at a low or medium level.
We have shown that rumen fungi endoglucanases of GH family 5 and xylanases of GH family 11 are more homologous to bacterial sequences than fungal ones. This is also true for almost every sequence in the GH group. Trees from GH families 6 and 10 were not as robust as trees from GH families 5 and 11, although the GHs of rumen fungi do not cluster with sequences from other fungi (results not shown). The mannanase sequences (manA, manB, and manC) from Piromyces sp. that are supposed to have arisen through gene duplication (Millward-Sadler et al. 1996
) belong to GH family 26, a family with only bacterial sequences and are approximately 50% similar to the catalytic domains of bacterial mannanases from Dictyoglomus thermophilum (TrEMBL code O30654), Caldicellulosiruptor saccharolyticus (SW code P77847), and Rhodotermus marinus (P49425). The lichenase licA from Orpinomyces sp. which belong to GH family 16 have the highest homology (60%–66% similarity) with bacterial lichenases from Streptococcus bovis (O07856), Paenibacillus polymyxa (P45797), Paenibacillus macerans (P23904), and Bacillus subtilis (P04957). The acetylxylan esterase bnaII from N. patriciarum is 46% similar to an unknown domain of the cellulase E from Clostridium thermocellum (P10477). The acetylxylan esterase bnaI from N. patriciarum is 70% similar to an unknown domain of the xylanase B from R. flavefaciens (Q52753). The acetylxylan esterase bnaI from N. patriciarum shows homology (77% similarity) only with the acetylxylan esterase (axeA) from Orpinomyces sp. Based on codon usage analysis, the axeA gene from Orpinomyces sp. belong to the non-GH group. This could mean that these differences have undergone different amelioration processes. The only sequence of the GH group that does not resemble bacterial sequences is cyclophilin B (cypB) from Orpinomyces sp. This sequence has a stronger resemblance to animal cyclophilines (Chou and Gasser 1997
), and it is supposed to have had an animal origin (Chen, Li, and Ljungdahl 1995
). On the other hand, trees constructed with the 18S ribosomal RNA and the enolase and beta-succinyl-CoA synthethase sequences clearly cluster the Neocallimastix genus with the fungus kingdom (results not shown), and the most homologous sequences of rumen fungus genes of the non-GH group are sequences from other eukaryotic fungi.
Our observation that the sequences from the GH group are more homologous to bacterial sequences and that the sequences from the non-GH group are more homologous to fungal sequences supports the hypothesis that all of the GHs of rumen fungi and other genes that play an important role in the degradation of cellulose and other plant polysaccharides are of bacterial origin and have been acquired by horizontal gene transfer. Such an acquisition would have happened prior to the divergence of actual Neocallimasticales fungi and would have conferred beneficial phenotypic capabilities which allowed these fungi to colonize a new habitat: the rumen of the herbivorous mammals for which cellulose and plant hemicellulose constitute the main raw nutritive substrate. The fact that rumen fungi are monophyletic in origin (Flint 1994
), in contrast to the remarkable diversity of rumen bacteria, along with the fact that the GHs of rumen fungi form a cellulosome-like structure only found in anaerobic bacteria, supports this hypothesis. The acquisition of a group of GH genes that form a cellulosome-like structure requires only a few gene transfers if the GH genes and other cellulosome components are in a structure of operons in the donor organism. Cellulase gene clusters have in fact been reported from Clostridium josui (Karita, Sakka, and Ohmiya 1997
) and Clostridium cellulolyticum (Mitsumori and Minato 1997
), where a scaffolding protein is localized upstream of different cellulase genes. Further speciation, gene duplication, and chromosomal rearrangements would have originated the GH genes that we now find in rumen fungi. In the codon usage analysis, the GH genes cluster with Orpinomyces sp. cyclophilin B, which is thought to have had an animal origin (Chen, Li, and Ljungdahl 1995
). We can therefore deduce that these genes have been ameliorated (Lawrence and Ochman 1998
) and that they have adjusted to the base composition and codon usage of the resident genome.
The celB, celD, xynA, bnaIII, and bnaI sequences from N. patriciarum; the celA and xyn3 sequences from N. frontalis; the celB29 and celB2 sequences from O. joyonii; the celB, celA, celC, and xynA sequences from Orpinomyces sp.; and the xynA, manB, manA, and manC sequences from Piromyces sp. possess a dockerin domain which is responsible for binding to the cellulosome. A recent study has shown that a hemicellulase from marine Vibrio sp. has a reiterated sequence similar to that of the rumen fungal dockerin domain (Tamaru et al. 1997
). This species or its ancestor could be the origin of the transferred GH genes, but we have found that the codon usage pattern of Vibrio sp. genes does not resemble that of rumen fungi GH (results not shown). This difference in the codon usage could be due to the amelioration process (Lawrence and Ochman 1998
). More sequences of this domain in other bacterial species are needed to know more about its origin. It has been recently suggested that F. succinogenes may have originated from the marine environment (Iyo and Forsberg 1999
). The increasingly close relationship between the marine and rumen environments may indicate a marine origin for ruminal microorganisms.
Orpinomyces joyonii celA endoglucanase consists of an N-terminal catalytic domain, two repeated regions linked by a short Ser-rich linker, and a domain of unknown function. The repeated region of celA is very similar to the noncatalytic domain of F. succinogenes cel-3 cellulase, although no apparent homology exists between their catalytic domains. This suggested to Liu et al. (1997)
that there was some evolutionary shuffling of endoglucanase domains among bacteria and fungi within the anaerobic ecosystem of the rumen. We showed in the Results section that the G+C content and codon usage of the O. joyonii celA gene are more similar to values for F. succinogenes genes than to those for the other GH of rumen fungi. This relationship also exists if only the catalytic domain of the celA gene is considered (results not shown), which suggests that a recent horizontal transfer of the complete celA gene from F. succinogenes to O. joyonii has occurred. The fact that the catalytic domain of the O. joyonii celA endoglucanase does not branch with any F. succinogenes endoglucanase could indicate that the orthologous sequence of the celA gene has not yet been sequenced in F. succinogenes. The different cluster of the O. joyonii celA gene and paralogous celB29 and celB2 genes in the phylogenetic tree of GH family 5 and the absence of a dockerin domain that binds to the cellulosome in the celA gene suggest that the origin of celA is different from that of the other GHs of rumen fungi.
In conclusion, we have shown the horizontal gene transfer of the O. joyonii celA gene from F. succinogenes or a related species. The lack of homology between the sequences of the GH group of rumen fungi and sequences from other fungi suggests that most, if not all, of the GHs of rumen fungi that play an important role in the degradation of cellulose and other plant polysaccharides have been acquired through horizontal gene transfer events. When more gene sequences from rumen fungi are available, we will know whether the difference in codon usage between GH and non-GH groups is due to differences in the level of expression, an alien origin of GH genes, or both effects.
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Acknowledgements |
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This work has not been awarded grants by any research-supporting institution. S.G.-V. has been the recipient of a fellowship (FI/96-7.030) from the Catalan Governmental Agency CIRIT (Generalitat de Catalunya). We thank Kevin Costello (from the Language Service of our University) for his help during the writing of the manuscript.
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Footnotes |
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Thomas H. Eickbush, Reviewing Editor
1 Abbreviation: GH, glycosyl hydrolase. 
2 Keywords: glycosyl hydrolases
horizontal gene transfer
codon usage
Pearson linear correlation coefficient
rumen fungi
3 Address for correspondence and reprints: A. Romeu, Universitat Rovira i Virgili, Facultat Química, Departament Bioquímica i Biotecnologia, Plaça Imperial Tàrraco, 1, E-43005 Tarragona, Spain. E-mail: romeu{at}quimica.urv.es
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