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Phylogenetic evidence for lateral gene transfer in the intestine of marine iguanas.

Nelson DM, Cann IK, Altermann E, Mackie RI - PLoS ONE (2010)

Bottom Line: The fosmids encoded four transposase-encoding genes and an integrase-encoding gene, suggesting their involvement in LGT.In addition, several coding genes likely involved in sugar transport were probably acquired through LGT.Our phylogenetic evidence suggests that LGT may be common among phylogenetically distinct members of the phylum Firmicutes inhabiting the intestinal tract of marine iguanas.

View Article: PubMed Central - PubMed

Affiliation: Appalachian Laboratory, University of Maryland Center for Environmental Science, Frostburg, Maryland, USA. dmnelson@al.umces.edu

ABSTRACT

Background: Lateral gene transfer (LGT) appears to promote genotypic and phenotypic variation in microbial communities in a range of environments, including the mammalian intestine. However, the extent and mechanisms of LGT in intestinal microbial communities of non-mammalian hosts remains poorly understood.

Methodology/principal findings: We sequenced two fosmid inserts obtained from a genomic DNA library derived from an agar-degrading enrichment culture of marine iguana fecal material. The inserts harbored 16S rRNA genes that place the organism from which they originated within Clostridium cluster IV, a well documented group that habitats the mammalian intestinal tract. However, sequence analysis indicates that 52% of the protein-coding genes on the fosmids have top BLASTX hits to bacterial species that are not members of Clostridium cluster IV, and phylogenetic analysis suggests that at least 10 of 44 coding genes on the fosmids may have been transferred from Clostridium cluster XIVa to cluster IV. The fosmids encoded four transposase-encoding genes and an integrase-encoding gene, suggesting their involvement in LGT. In addition, several coding genes likely involved in sugar transport were probably acquired through LGT.

Conclusion: Our phylogenetic evidence suggests that LGT may be common among phylogenetically distinct members of the phylum Firmicutes inhabiting the intestinal tract of marine iguanas.

Show MeSH
Phylogenetic relationships of 16S rRNA gene sequences among the fosmids, clone library, and Clostridium clusters.Clone library sequences start with “M.” The numbers in parentheses following some of the marine iguana sequences indicate the number of times that a particular sequence was obtained. Only representatives of the major Clostridium clusters, and limited representatives of the Bacteroidetes and Coriobacteriales, are shown. The tree was inferred using the neighbor joining approach. The numbers at the nodes represent bootstrap values. The bar represents 0.02 substitutions per nucleotide position. The outgroup is Aquifex pyrophilus.
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pone-0010785-g001: Phylogenetic relationships of 16S rRNA gene sequences among the fosmids, clone library, and Clostridium clusters.Clone library sequences start with “M.” The numbers in parentheses following some of the marine iguana sequences indicate the number of times that a particular sequence was obtained. Only representatives of the major Clostridium clusters, and limited representatives of the Bacteroidetes and Coriobacteriales, are shown. The tree was inferred using the neighbor joining approach. The numbers at the nodes represent bootstrap values. The bar represents 0.02 substitutions per nucleotide position. The outgroup is Aquifex pyrophilus.

Mentions: In order to compete for resources and ultimately, to allow their host to survive and reproduce, intestinal microorganisms must also adapt. An emerging theme in genomic biology suggests that lateral gene transfer (LGT) is key for promoting genotypic and phenotypic variation in microorganisms [7], including those from intestinal environments [8], [9], [10], [11]. For example, Ricard et al. (2006) showed that ∼4% of genes in the genomes of ciliates common in the rumen were likely obtained from bacteria and archaea [11]. The majority of these genes were involved with carbohydrate catabolism, suggesting that their acquisition helped ciliates to successfully colonize and adapt to the rumen environment. Although the extent and control of LGT among microorganisms in the intestine of non-mammalian hosts, such as reptiles, remains unexplored, 16S rDNA clone libraries suggest that their gut bacterial communities differ in composition from those of herbivorous mammals. Firmicutes and specifically several phylogenetically defined Clostridium clusters (I, III, IV, and XIVa) are the predominant phyla in the intestine of marine iguanas (Amblyrynchus cristatus; Fig. 1) [4], land iguanas (Conolophus spp.), and giant tortoises (Testudo elephantopus) (Mackie, unpublished data). In contrast, herbivorous mammals also contain an abundance of diverse representatives of the phylum Bacteroidetes [12]. Thus if LGT is an important process in the intestine of herbivorous reptiles, it likely occurs among non-Bacteroidetes species.


Phylogenetic evidence for lateral gene transfer in the intestine of marine iguanas.

Nelson DM, Cann IK, Altermann E, Mackie RI - PLoS ONE (2010)

Phylogenetic relationships of 16S rRNA gene sequences among the fosmids, clone library, and Clostridium clusters.Clone library sequences start with “M.” The numbers in parentheses following some of the marine iguana sequences indicate the number of times that a particular sequence was obtained. Only representatives of the major Clostridium clusters, and limited representatives of the Bacteroidetes and Coriobacteriales, are shown. The tree was inferred using the neighbor joining approach. The numbers at the nodes represent bootstrap values. The bar represents 0.02 substitutions per nucleotide position. The outgroup is Aquifex pyrophilus.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2875401&req=5

pone-0010785-g001: Phylogenetic relationships of 16S rRNA gene sequences among the fosmids, clone library, and Clostridium clusters.Clone library sequences start with “M.” The numbers in parentheses following some of the marine iguana sequences indicate the number of times that a particular sequence was obtained. Only representatives of the major Clostridium clusters, and limited representatives of the Bacteroidetes and Coriobacteriales, are shown. The tree was inferred using the neighbor joining approach. The numbers at the nodes represent bootstrap values. The bar represents 0.02 substitutions per nucleotide position. The outgroup is Aquifex pyrophilus.
Mentions: In order to compete for resources and ultimately, to allow their host to survive and reproduce, intestinal microorganisms must also adapt. An emerging theme in genomic biology suggests that lateral gene transfer (LGT) is key for promoting genotypic and phenotypic variation in microorganisms [7], including those from intestinal environments [8], [9], [10], [11]. For example, Ricard et al. (2006) showed that ∼4% of genes in the genomes of ciliates common in the rumen were likely obtained from bacteria and archaea [11]. The majority of these genes were involved with carbohydrate catabolism, suggesting that their acquisition helped ciliates to successfully colonize and adapt to the rumen environment. Although the extent and control of LGT among microorganisms in the intestine of non-mammalian hosts, such as reptiles, remains unexplored, 16S rDNA clone libraries suggest that their gut bacterial communities differ in composition from those of herbivorous mammals. Firmicutes and specifically several phylogenetically defined Clostridium clusters (I, III, IV, and XIVa) are the predominant phyla in the intestine of marine iguanas (Amblyrynchus cristatus; Fig. 1) [4], land iguanas (Conolophus spp.), and giant tortoises (Testudo elephantopus) (Mackie, unpublished data). In contrast, herbivorous mammals also contain an abundance of diverse representatives of the phylum Bacteroidetes [12]. Thus if LGT is an important process in the intestine of herbivorous reptiles, it likely occurs among non-Bacteroidetes species.

Bottom Line: The fosmids encoded four transposase-encoding genes and an integrase-encoding gene, suggesting their involvement in LGT.In addition, several coding genes likely involved in sugar transport were probably acquired through LGT.Our phylogenetic evidence suggests that LGT may be common among phylogenetically distinct members of the phylum Firmicutes inhabiting the intestinal tract of marine iguanas.

View Article: PubMed Central - PubMed

Affiliation: Appalachian Laboratory, University of Maryland Center for Environmental Science, Frostburg, Maryland, USA. dmnelson@al.umces.edu

ABSTRACT

Background: Lateral gene transfer (LGT) appears to promote genotypic and phenotypic variation in microbial communities in a range of environments, including the mammalian intestine. However, the extent and mechanisms of LGT in intestinal microbial communities of non-mammalian hosts remains poorly understood.

Methodology/principal findings: We sequenced two fosmid inserts obtained from a genomic DNA library derived from an agar-degrading enrichment culture of marine iguana fecal material. The inserts harbored 16S rRNA genes that place the organism from which they originated within Clostridium cluster IV, a well documented group that habitats the mammalian intestinal tract. However, sequence analysis indicates that 52% of the protein-coding genes on the fosmids have top BLASTX hits to bacterial species that are not members of Clostridium cluster IV, and phylogenetic analysis suggests that at least 10 of 44 coding genes on the fosmids may have been transferred from Clostridium cluster XIVa to cluster IV. The fosmids encoded four transposase-encoding genes and an integrase-encoding gene, suggesting their involvement in LGT. In addition, several coding genes likely involved in sugar transport were probably acquired through LGT.

Conclusion: Our phylogenetic evidence suggests that LGT may be common among phylogenetically distinct members of the phylum Firmicutes inhabiting the intestinal tract of marine iguanas.

Show MeSH