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Grafting or pruning in the animal tree: lateral gene transfer and gene loss?

ABSTRACT: BACKGROUND:Lateral gene transfer (LGT), also known as horizontal gene transfer, into multicellular eukaryotes with differentiated tissues, particularly gonads, continues to be met with skepticism by many prominent evolutionary and genomic biologists. A detailed examination of 26 animal genomes identified putative LGTs in invertebrate and vertebrate genomes, concluding that there are fewer predicted LGTs in vertebrates/chordates than invertebrates, but there is still evidence of LGT into chordates, including humans. More recently, a reanalysis of a subset of these putative LGTs into vertebrates concluded that there is not horizontal gene transfer in the human genome. One of the genes in dispute is an N-acyl-aromatic-L-amino acid amidohydrolase (ENSG00000132744), which encodes ACY3. This gene was initially identified as a putative bacteria-chordate LGT but was later debunked as it has a significant BLAST match to a more recently deposited genome of Saccoglossus kowalevskii, a flatworm, Metazoan, and hemichordate. RESULTS:Using BLAST searches, HMM searches, and phylogenetics to assess the evidence for LGT, gene loss, and rate variation in ACY3/ASPA homologues, the most parsimonious explanation for the distribution of ACY3/ASPA genes in eukaryotes involves both gene loss and bacteria-animal LGT, albeit LGT that occurred hundreds of millions of years ago prior to the divergence of gnathostomes. CONCLUSIONS:ACY3/ASPA is most likely a bacteria-animal LGT. LGTs at these time scales in the ancestors of humans are not unexpected given the many known, well-characterized, and adaptive LGTs from bacteria to insects and nematodes.

SUBMITTER: Dunning Hotopp JC

PROVIDER: S-EPMC6006793 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Grafting or pruning in the animal tree: lateral gene transfer and gene loss?

Dunning Hotopp Julie C JC

BMC genomics 20180618 1

<h4>Background</h4>Lateral gene transfer (LGT), also known as horizontal gene transfer, into multicellular eukaryotes with differentiated tissues, particularly gonads, continues to be met with skepticism by many prominent evolutionary and genomic biologists. A detailed examination of 26 animal genomes identified putative LGTs in invertebrate and vertebrate genomes, concluding that there are fewer predicted LGTs in vertebrates/chordates than invertebrates, but there is still evidence of LGT into ...[more]

PMID: 29914363

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Project description:BACKGROUND: Aphids possess bacteriocytes, which are cells specifically differentiated to harbour the obligate mutualist Buchnera aphidicola (gamma-Proteobacteria). Buchnera has lost many of the genes that appear to be essential for bacterial life. From the bacteriocyte of the pea aphid Acyrthosiphon pisum, we previously identified two clusters of expressed sequence tags that display similarity only to bacterial genes. Southern blot analysis demonstrated that they are encoded in the aphid genome. In this study, in order to assess the possibility of lateral gene transfer, we determined the full-length sequences of these transcripts, and performed detailed structural and phylogenetic analyses. We further examined their expression levels in the bacteriocyte using real-time quantitative RT-PCR. RESULTS: Sequence similarity searches demonstrated that these fully sequenced transcripts are significantly similar to the bacterial genes ldcA (product, LD-carboxypeptidase) and rlpA (product, rare lipoprotein A), respectively. Buchnera lacks these genes, whereas many other bacteria, including Escherichia coli, a close relative of Buchnera, possess both ldcA and rlpA. Molecular phylogenetic analysis clearly demonstrated that the aphid ldcA was derived from a rickettsial bacterium closely related to the extant Wolbachia spp. (alpha-Proteobacteria, Rickettsiales), which are intracellular symbionts of various lineages of arthropods. The evolutionary origin of rlpA was not fully resolved, but it was clearly demonstrated that its double-psi beta-barrel domain is of bacterial origin. Real-time quantitative RT-PCR demonstrated that ldcA and rlpA are expressed 11.6 and 154-fold higher in the bacteriocyte than in the whole body, respectively. LdcA is an enzyme required for recycling murein (peptidoglycan), which is a component of the bacterial cell wall. As Buchnera possesses a cell wall composed of murein but lacks ldcA, a high level of expression of the aphid ldcA in the bacteriocyte may be essential to maintain Buchnera. Although the function of RlpA is not well known, conspicuous up-regulation of the aphid rlpA in the bacteriocyte implies that this gene is also essential for Buchnera. CONCLUSION: In this study, we obtained several lines of evidence indicating that aphids acquired genes from bacteria via lateral gene transfer and that these genes are used to maintain the obligately mutualistic bacterium, Buchnera.

Project description:Gardnerella spp. are pathognomonic for bacterial vaginosis, which increases the risk of preterm birth and the transmission of sexually transmitted infections. Gardnerella spp. are genetically diverse, comprising what have recently been defined as distinct species with differing functional capacities. Disease associations with Gardnerella spp. are not straightforward: patients with BV are usually infected with multiple species, and Gardnerella spp. are also found in the vaginal microbiome of healthy women. Genome comparisons of Gardnerella spp. show evidence of lateral gene transfer (LGT), but patterns of LGT have not been characterized in detail. Here we sought to define the role of LGT in shaping the genetic structure of Gardnerella spp. We analyzed whole genome sequencing data for 106 Gardnerella strains and used these data for pan genome analysis and to characterize LGT in the core and accessory genomes, over recent and remote timescales. In our diverse sample of Gardnerella strains, we found that both the core and accessory genomes are clearly differentiated in accordance with newly defined species designations. We identified putative competence and pilus assembly genes across most species; we also found them to be differentiated between species. Competence machinery has diverged in parallel with the core genome, with selection against deleterious mutations as a predominant influence on their evolution. By contrast, the virulence factor vaginolysin, which encodes a toxin, appears to be readily exchanged among species. We identified five distinct prophage clusters in Gardnerella genomes, two of which appear to be exchanged between Gardnerella species. Differences among species are apparent in their patterns of LGT, including their exchange with diverse gene pools. Despite frequent LGT and co-localization in the same niche, our results show that Gardnerella spp. are clearly genetically differentiated and yet capable of exchanging specific genetic material. This likely reflects complex interactions within bacterial communities associated with the vaginal microbiome. Our results provide insight into how such interactions evolve and are maintained, allowing these multi-species communities to colonize and invade human tissues and adapt to antibiotics and other stressors.

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Grafting or pruning in the animal tree: lateral gene transfer and gene loss?

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Grafting or pruning in the animal tree: lateral gene transfer and gene loss?

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