Strict Vertical Transmission Research Articles

Dispersion and colonisation by fungus-growing termites

The fungus-growing termites (Macrotermitinae) have developed an obligate mutualistic symbiosis with fungi (Termitomyces) and, in most cases, the symbiotic partner is collected from the environment upon establishment of a new colony (horizontal transmission). The requirement that partners are able to find and recognize each other after independent reproduction is likely to severely constrain long distance dispersal. In supports of this hypothesis, we have recently shown that a single colonisation of Madagascar by fungus-growing termites has occurred. The successful colonizers belong to the genus Microtermes, known to inherit their symbiont from the parental colony (vertical transmission). However, the fungal symbionts of Madagascar were not monophyletic, as expected under strict vertical transmission. Here we further discuss these findings, and we suggest further bottlenecks to dispersion and propose a transient window for horizontal transmission for the otherwise vertically transmitted Termitomyces strains.

Pyrosequencing analysis of endosymbiont population structure: co‐occurrence of divergent symbiont lineages in a single vesicomyid host clam

Bacteria-eukaryote endosymbioses are perhaps the most pervasive co-evolutionary associations in nature. Here, intracellular chemosynthetic symbionts of deep-sea clams (Vesicomyidae) were analysed by amplicon pyrosequencing to explore how symbiont transmission mode affects the genetic diversity of the within-host symbiont population. Vesicomyid symbionts (Gammaproteobacteria) are presumed to be obligately intracellular, to undergo nearly strict vertical transmission between host generations, and to be clonal within a host. However, recent data show that vesicomyid symbionts can be acquired laterally via horizontal transfer between hosts or uptake from the environment, potentially creating opportunities for multiple symbiont strains to occupy the same host. Here, genotype-specific PCR and direct sequencing of the bacterial internal transcribed spacer initially demonstrated the co-occurrence of two symbiont strains, symA and symB (93.5% nt identity), in 8 of 118 Vesicomya sp. clams from 3 of 7 hydrothermal vent sites on the Juan de Fuca Ridge. To confirm multiple strains within individual clams, amplicon pyrosequencing of two symbiont loci was used to obtain deep-coverage measurements (mean: approximately 1500x coverage per locus per clam) of symbiont population structure. Pyrosequencing confirmed symA-symB co-occurrence for two individuals, showing the presence of both genotypes in amplicon pools. However, in the majority of clams, the endosymbiont population was remarkably homogenous, with > 99.5% of sequences collapsing into a single symbiont genotype in each clam. These results support the hypothesis that a predominantly vertical transmission strategy leads to the fixation of a single symbiont strain in most hosts. However, mixed symbiont populations do occur in vesicomyids, potentially facilitating the exchange of genetic material between divergent symbiont lineages.

Yeasts Isolated from Neotropical Wood‐Boring Beetles in SE Peru

ABSTRACTSome temperate wood‐boring cerambycid beetles harbor intracellular gut yeasts believed to augment host nutrition, but species belonging to the subfamily Lamiinae are thought to lack endosymbionts. Almost 49 percent of Neotropical cerambycid species are lamiines, therefore, comparatively few rain forest species would be expected to host symbiotic gut yeasts. This study reports the isolation of gut yeasts from closely related Neotropical lamiines. We investigated species that feed on trees in the Brazil nut family (Lecythidaceae), because host plant associations are relatively well known. Our objectives were to determine if gut yeasts were present and, if possible, infer their mode of transmission. We collected and dissected 18 beetle specimens from three tree species, including 17 cerambycids and one curculionid. Every insect specimen yielded a gut yeast. DNA sequence libraries were used for a rapid identification of the yeasts and their larval hosts. The cerambycids included five lamiine species and one cerambycine. Six ascomycete yeasts were isolated from their guts; we found no evidence of strict vertical transmission. Larval gut yeasts were genetically similar to yeasts previously isolated from insects associated with wood or fungi, implying potential habitat specificity. The yeasts have not yet been localized, and potential function is not known, but they may contribute to rapid nutrient cycling or serve as the first line of defense against plant toxins.

The Juan non-LTR retrotransposon in mosquitoes: genomic impact, vertical transmission and indications of recent and widespread activity

BackgroundIn contrast to DNA-mediated transposable elements (TEs), retrotransposons, particularly non-long terminal repeat retrotransposons (non-LTRs), are generally considered to have a much lower propensity towards horizontal transfer. Detailed studies on site-specific non-LTR families have demonstrated strict vertical transmission. More studies are needed with non-site-specific non-LTR families to determine whether strict vertical transmission is a phenomenon related to site specificity or a more general characteristic of all non-LTRs. Juan is a Jockey clade non-LTR retrotransposon first discovered in mosquitoes that is widely distributed in the mosquito family Culicidae. Being a non-site specific non-LTR, Juan offers an opportunity to further investigate the hypothesis that non-LTRs are genomic elements that are primarily vertically transmitted.ResultsSystematic analysis of the ~1.3 Gbp Aedes aegypti (Ae. aegypti) genome sequence suggests that Juan-A is the only Juan-type non-LTR in Aedes aegypti. Juan-A is highly reiterated and comprises approximately 3% of the genome. Using minimum cutoffs of 90% length and 70% nucleotide (nt) identity, 663 copies were found by BLAST using the published Juan-A sequence as the query. All 663 copies are at least 95% identical to Juan-A, while 378 of these copies are 99% identical to Juan-A, indicating that the Juan-A family has been transposing recently in evolutionary history. Using the 0.34 Kb 5' UTR as the query, over 2000 copies were identified that may contain internal promoters, leading to questions on the genomic impact of Juan-A. Juan sequences were obtained by PCR, library screening, and database searches for 18 mosquito species of six genera including Aedes, Ochlerotatus, Psorophora, Culex, Deinocerites, and Wyeomyia. Comparison of host and Juan phylogenies shows overall congruence with few exceptions.ConclusionJuan-A is a major genomic component in Ae. aegypti and it has been retrotransposing recently in evolutionary history. There are also indications that Juan has been recently active in a wide range of mosquito species. Furthermore, our research demonstrates that a Jockey clade non-LTR without target site-specificity has been sustained by vertical transmission in the mosquito family. These results strengthen the argument that non-LTRs tend to be genomic elements capable of persistence by vertical descent over a long evolutionary time.

A Population Genetics Pedigree Perspective on the Transmission of Helicobacter pylori

The inference of transmission pathways for medicinally important bacteria is important to our understanding of pathogens. Here we report analyses of transmission in Helicobacter pylori, a major carcinogen. Our study is novel in that the focal community comprises detailed family pedigrees and has a high prevalence of H. pylori. To infer transmission, we performed high-resolution analyses of nucleotide sequences for three genes and accounted for the occurrence of mutation and recombination through the use of simulation modeling. Our results demonstrate that transmission has a strong nonfamilial component potentially the result of a large proportion of infections derived from the community. These results are interesting from both a medical and an evolutionary standpoint. First, efficient control measures and beliefs about the sources of H. pylori infection should be reevaluated. Evolutionarily, our results contradict the hypothesis of strict vertical transmission, presented as an explanation for the strong correlation between human population history and H. pylori diversity. Thus the paradox of persistent phylogenetic structure, despite a permissive mode of transmission and high recombination rates, must be solved elsewhere. Here we consider the potential for recombination events to maintain genetic structure in light of horizontal transmission.

Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis.

The fungus-growing ants have long provided a spectacular example of coevolutionary integration. Their ecological success is thought to depend largely on the evolutionary alignment of reproductive interests between ants and fungi after vertical transmission and the ancient suppression of fungal sexuality. In the present study we test these assumptions and provide the first evidence of recombination in attine cultivars, contradicting widely held perceptions of obligate clonality. In addition, we document long-distance horizontal transmission of symbionts between leaf-cutter ant species on mainland Central America and South America and those endemic to Cuba, suggesting both lack of pairwise coevolutionary specificity in ant/cultivar interactions and dispersal of symbionts independent of their ant hosts. The coevolution between leaf-cutters and their fungal symbionts is thus not reciprocally pairwise. Rather, a single widespread and sexual fungal symbiont species is engaged in multiple interactions with divergent ant lineages. Strict fungal clonality and vertical transmission evidently have not played a critical role in the long-term evolutionary or ecological success of this well known mutualism.

Phylogenomic analysis of chromoviruses

Genome sequences of model organisms provide a unique opportunity to obtain insight into the complete diversity of any transposable element (TE) group. A limited number of chromoviruses, the chromodomain containing genus of Metaviridae, is known from plant, fungal and vertebrate genomes. By searching diverse eukaryotic genome databases, we have found a surprisingly large number of new, structurally intact and highly conserved chromoviral elements, greatly exceeding the number of previously known chromoviruses. In this study, we examined the diversity, origin and evolution of chromoviruses in Eukaryota. Chromoviral diversity in plants, fungi and vertebrates, as shown by phylogenetic analyses, was found to be much greater than previously expected. A novel centromere-specific chromoviral lineage was found to be widespread and highly conserved in all seed plants. The age of chromoviruses has been significantly extended by finding their representatives in the most basal plant lineages (green and red algae), in Heterokonta (oomycetes) and in Cercozoa (plasmodiophorids). The evolutionary origin of chromoviruses has been found to be no earlier than in Cercozoa, since none can be found in the basal eukaryotic lineages, despite the extensive genome data. The evolutionary dynamics of chromoviruses can be explained by a strict vertical transmission in plants and fungi, while in Metazoa it is more complex. The currently available genome data clearly show that chromoviruses are the most widespread and one of the oldest Metaviridae clade.

Adaptive evolution in GroEL from distantly related endosymbiotic bacteria of insects

Many symbioses between bacteria and insects resulted from ancient infections followed by strict vertical transmission within host lineages. The strong bottlenecks under which this transmission occurs promote the neutral fixation of slightly deleterious mutations by genetic drift. As predicted by Muller's ratchet, this fixation will drive endosymbiotic bacteria through an irreversible dynamics of fitness loss. The chaperonin GroEL has been proposed as a compensatory mechanism whereby endosymbiotic bacteria of aphids persist. Here, we show that endosymbiotic bacteria of insects from two phylogenetically very distant bacterial phyla have fixed amino acid substitutions by positive selection in functionally important GroEL regions involved in either GroES/peptide binding or in the en bloc movement of the GroEL apical domain. These results, together with the high levels of constitutive expression of GroEL in these endosymbionts, provide valuable insights into the evolution of a molecular mechanism responsible for the maintenance of the symbiotic lifestyle.

Evolutionary Genomics of Chromoviruses in Eukaryotes

The diversity, origin, and evolution of chromoviruses in Eukaryota were examined using the massive amount of genome sequence data for different eukaryotic lineages. A surprisingly large number of novel full-length chromoviral elements were found, greatly exceeding the number of the known chromoviruses. These new elements are mostly structurally intact and highly conserved. Chromoviruses in the key Amniota lineage, the reptiles, have been analyzed by PCR to explain their evolutionary dynamics in amniotes. Phylogenetic analyses provide evidence for a novel centromere-specific chromoviral clade that is widespread and highly conserved in all seed plants. Chromoviral diversity in plants, fungi, and vertebrates, as shown by phylogenetic analyses, was found to be much greater than previously expected. The age of plant chromoviruses has been significantly extended by finding their representatives in the most basal plant lineages, the green and the red algae. The evolutionary origin of chromoviruses has been found to be no earlier than in Cercozoa. The evolutionary history and dynamics of chromoviruses can be explained simply by strict vertical transmission in plants, followed by more complex evolution in fungi and in Metazoa. The currently available data clearly show that chromoviruses indeed represent the oldest and the most widespread clade of Metaviridae.

Phylogeny and self-splicing ability of the plastid tRNA-Leu group I Intron.

Group I introns are mobile RNA enzymes (ribozymes) that encode conserved primary and secondary structures required for autocatalysis. The group I intron that interrupts the tRNA-Leu gene in cyanobacteria and plastids is remarkable because it is the oldest known intervening sequence and may have been present in the common ancestor of the cyanobacteria (i.e., 2.7-3.5 billion years old). This intron entered the eukaryotic domain through primary plastid endosymbiosis. We reconstructed the phylogeny of the tRNA-Leu intron and tested the in vitro self-splicing ability of a diverse collection of these ribozymes to address the relationship between intron stability and autocatalysis. Our results suggest that the present-day intron distribution in plastids is best explained by strict vertical transmission, with no intron losses in land plants or a subset of the Stramenopiles (xanthophyceae/phaeophyceae) and frequent loss among green algae, as well as in the red algae and their secondary plastid derivatives (except the xanthophyceae/phaeophyceae lineage). Interestingly, all tested land plant introns could not self-splice in vitro and presumably have become dependent on a host factor to facilitate in vivo excision. The host dependence likely evolved once in the common ancestor of land plants. In all other plastid lineages, these ribozymes could either self-splice or complete only the first step of autocatalysis.

Intracellular symbionts of sharpshooters (Insecta: Hemiptera: Cicadellinae) form a distinct clade with a small genome.

The leafhoppers (Insecta: Hemiptera: Cicadellidae) are the most species-rich group of invertebrates in which intracellular symbionts are usual. Here we present the first molecular characterization of bacteriome-associates in the leafhoppers, with focus on the subfamily Cicadellinae (sharpshooters). Phylogenetic analyses of 16S rDNA sequences from intracellular symbionts residing in the bacteriomes of five host species indicate that these symbionts form a well-defined clade within the gamma-3 Proteobacteria, consistent with an ancient colonization and strict vertical transmission. More extensive gene sequence information is reported for the symbiont of Homalodisca coagulata (Say). The genome size, as determined by pulsed field gel electrophoresis, is approximately 680 kb. This finding, when combined with published results for symbionts of aphids, ants, psyllids and tsetse flies, adds to an emerging pattern which suggests that bacteriome associates often descend from ancient infections by gamma Proteobacteria, and that these lineages have undergone pronounced genome reduction. A new genus and species name, 'Candidatus Baumannia cicadellinicola' (sp. nov.) is proposed for this newly characterized clade of symbiotic bacteria.

Evolutionary dynamics in a novel L2 clade of non-LTR retrotransposons in Deuterostomia.

The evolution of the novel L2 clade of non-long terminal repeat (LTR) retrotransposons and their evolutionary dynamics in Deuterostomia has been examined. The short-term evolution of long interspersed nuclear element 2s (LINE2s) has been studied in 18 reptilian species by analysis of a PCR amplified 0.7-kb fragment encoding the palm/fingers subdomain of reverse transcriptase (RT). Most of the reptilian LINE2s examined are inactive since they contain multiple stop codons, indels, or frameshift mutations that disrupt the RT. Analysis of reptilian LINE2s has shown a high degree of sequence divergence and an unexpectedly large number of deletions. The evolutionary dynamics of LINE2s in reptiles has been found to be complex. LINE2s are shown to form a novel clade of non-LTR retrotransposons that is well separated from the CR1 clade. This novel L2 clade is more widely distributed than previously thought, and new representatives have been discovered in echinoderms, insects, teleost fishes, Xenopus, Squamata, and marsupials. There is an apparent absence of LINE2s from different vertebrate classes, such as cartilaginous fishes, Archosauria (birds and crocodiles), and turtles. Whereas the LINE2s are present in echinoderms and teleost fishes in a conserved form, in most tetrapods only highly degenerated pseudogenes can be found. The predominance of inactive LINE2s in Tetrapoda indicates that, in the host genomes, only inactive copies are still present. The present data indicate that the vertical inactivation of LINE2s might have begun at the time of Tetrapoda origin, 400 MYA. The evolutionary dynamics of the L2 clade in Deuterostomia can be described as a gradual vertical inactivation in Tetrapoda, stochastic loss in Archosauria and turtles, and strict vertical transmission in echinoderms and teleost fishes.

Sequences homologous to Tc(s) transposable elements of Caenorhabditis elegans are widely distributed in the phylum nematoda.

To have a better understanding of the evolutionary history of mobile elements within the nematodes, we examined the distribution and the conservation of homologues to transposable elements from Caenorhabditis elegans (Tc1, Tc2, Tc3, Tc4, Tc5, and FB1) in 19 nematode species belonging to the class Secernentea. Our results show that Tc1 elements display a distribution restricted to the family Rhabditidae with poor conservation. The Tc2 and FB1 homologous elements have the same patchy distribution within the Rhabditidae. They were only found in Caenorhabditis and in Teratorhabditis. The Tc3 element is widely distributed among nematode species. Tc3 homologous elements are present in the majority of the Rhabditidae but also in two genera within the family Panagrolaimidae, and in Bursaphelenchus, which belongs to the order Aphelenchida. Tc4 and Tc5 homologues show the most limited distribution of all tested elements, being strictly limited to C. elegans. These data indicate that in some cases, the distribution of transposable elements in the nematode cannot be explained by strict vertical transmission. The distribution of Tc3, Tc4, and Tc5 suggests that horizontal transmission may have occurred between reproductively isolated species during their evolutionary history.