Symbiont genes in host genomes: fragments with a future?

While lateral transfer is the rule in the evolutionary history of bacterial and archaeal genes, events of transfer from prokaryotes to eukaryotes are rare. Germline-transmitted animal symbionts, such as Wolbachia pipientis, are well placed to participate in such transfers. In a recent issue of Science, Dunning Hotopp et al. identified instances of transfer of Wolbachia DNA to host genomes. It is unknown whether these transfers represent innovation in animal evolution.     

Ancient gene transfer from algae to animals: Mechanisms and evolutionary significance

ABSTRACT: BACKGROUND: Horizontal gene transfer (HGT) is traditionally considered to be rare in multicellular eukaryotes such as animals. Recently, many genes of miscellaneous algal origins were discovered in choanoflagellates. Considering that choanoflagellates are the existing closest relatives of animals, we speculated that ancient HGT might have occurred in the unicellular ancestor of animals and affected the long-term evolution of animals. RESULTS: Through genome screening, phylogenetic and domain analyses, we identified 14 gene families, including 92 genes, in the tunicate Ciona intestinalis that are likely derived from miscellaneous photosynthetic eukaryotes. Almost all of these gene families are distributed in diverse animals, suggesting that they were mostly acquired by the common ancestor of animals. Their miscellaneous origins also suggest that these genes are not derived from a particular algal endosymbiont. In addition, most genes identified in our analyses are functionally related to molecule transport, cellular regulation and methylation signaling, suggesting that the acquisition of these genes might have facilitated the intercellular communication in the ancestral animal. CONCLUSIONS: Our findings provide additional evidence that algal genes in aplastidic eukaryotes are not exclusively derived from historical plastids and thus important for interpreting the evolution of eukaryotic photosynthesis. Most importantly, our data represent the first evidence that more anciently acquired genes might exist in animals and that ancient HGT events have played an important role in animal evolution.     

Comparative study of vanA gene transfer from Enterococcus faecium to Enterococcus faecalis and to Enterococcus faecium in the intestine of mice

Vancomycin-resistant enterococci represent a large reservoir in animals because of the use of avoparcin as a growth promoter in Europe. These strains of animal origin enter the food chain and can either colonize the human gut or transfer their resistance genes to the human microbiota. In this study, we compared the transfer of vancomycin resistance from resistant animal Enterococcus faecium to sensitive human Enterococcus faecalis and E. faecium. We analysed these transfers in dibiotic mice and human faecal flora-associated mice. VanA transfer from animal E. faecium to human E. faecalis occurred in dibiotic mice. The transconjugants appeared rapidly and persisted at levels between 3.0 and 4.0 log10 colony-forming units g(-1) of faeces. In human faecal flora-associated mice, vanA gene transfer was not detected towards E. faecalis but was possible between E. faecium strains. Our experiments revealed the possibility of vanA transfer from animal E. faecium to human E. faecalis in vitro and in vivo in the intestine of dibiotic mice. However, intraspecies transfer of vanA gene seems more common than interspecies transfer among enterococci.     

Adaptive eukaryote-to-eukaryote lateral gene transfer: stress-related genes of algal origin in the closest unicellular relatives of animals

In addition to mutation, gene duplication and recombination, the transfer of genetic material between unrelated species is now regarded as a potentially significant player in the shaping of extant genomes and the evolution and diversification of life. Although this is probably true for prokaryotes, the extent of such genetic exchanges in eukaryotes (especially eukaryote-to-eukaryote transfers) is more controversial and the selective advantage and evolutionary impact of such events are less documented. A laterally transferred gene could either be added to the gene complement of the recipient or replace the recipient's homologue; whereas gene replacements can be either adaptive or stochastic, gene additions are most likely adaptive. Here, we report the finding of four stress-related genes (two ascorbate peroxidase and two metacaspase genes) of algal origin in the closest unicellular relatives of animals, the choanoflagellates. At least three of these sequences represent additions to the choanoflagellate gene complement, which is consistent with these transfers being adaptive. We suggest that these laterally acquired sequences could have provided the primitive choanoflagellates with additional or more efficient means to cope with stress, especially in relation to adapting to freshwater environments and/or sessile or colonial lifestyles.     

Horizontal gene transfer in the acquisition of novel traits by metazoans

Horizontal gene transfer is accepted as an important evolutionary force modulating the evolution of prokaryote genomes. However, it is thought that horizontal gene transfer plays only a minor role in metazoan evolution. In this paper, I critically review the rising evidence on horizontally transferred genes and on the acquisition of novel traits in metazoans. In particular, I discuss suspected examples in sponges, cnidarians, rotifers, nematodes, molluscs and arthropods which suggest that horizontal gene transfer in metazoans is not simply a curiosity. In addition, I stress the scarcity of studies in vertebrates and other animal groups and the importance of forthcoming studies to understand the importance and extent of horizontal gene transfer in animals.     

Using embryonic stem cells to introduce mutations into the mouse germ line

It is now possible, through the use of a number of experimental technologies, to transfer genetic information into mouse embryos to stably alter the genetic constitution of mice. This experimental approach, namely the generation of so-termed "transgenic" animals, is affording new insights into a wide variety of biological problems. This review focuses on one system for the generation of transgenic mice, which utilizes tissue culture cell lines of embryonic stem cells, termed ES cells. The remarkable property of ES cells is that they retain the potential to reform an embryo; when they are replaced inside a carrier embryo, they resume normal development and contribute to all the tissues of the live-born chimeric animal. Recent experiments, using a repertoire of gene transfer techniques, have shown that ES cells are amenable to a variety of experimental manipulations in tissue culture. Moreover, it has been demonstrated that these genetically altered cells can be transferred into the germ line of chimeric mice, thus allowing the production of unique strains of animals for study. The applications of the ES cell system are reviewed, with particular emphasis on their use for the generation of random insertional mutations using a retrovirally mediated mutagenesis approach. Finally, the use of ES cells in conjunction with the recently described technique of homologous recombination, or "gene targeting," is discussed. This technology allows the generation of animals carrying extremely precise genetic modifications of endogenous genes.     

Evolutionary analyses of the small subunit of glutamate synthase: gene order conservation,gene fusions,and prokaryote-to-eukaryote lateral gene transfers

Lateral gene transfer has been identified as an important mode of genome evolution within prokaryotes. Except for the special case of gene transfer from organelle genomes to the eukaryotic nucleus, only a few cases of lateral gene transfer involving eukaryotes have been described. Here we present phylogenetic and gene order analyses on the small subunit of glutamate synthase (encoded by gltD) and its homologues, including the large subunit of sulfide dehydrogenase (encoded by sudA). The scattered distribution of the sudA and sudB gene pair and the phylogenetic analysis strongly suggest that lateral gene transfer was involved in the propagation of the genes in the three domains of life. One of these transfers most likely occurred between a prokaryote and an ancestor of diplomonad protists. Furthermore, phylogenetic analyses indicate that the gene for the small subunit of glutamate synthase was transferred from a low-GC gram-positive bacterium to a common ancestor of animals, fungi, and plants. Interestingly, in both examples, the eukaryotes encode a single gene that corresponds to a conserved operon structure in prokaryotes. Our analyses, together with several recent publications, show that lateral gene transfers from prokaryotes to unicellular eukaryotes occur with appreciable frequency. In the case of the genes for sulfide dehydrogenase, the transfer affected only a limited group of eukaryotes—the diplomonads—while the transfer of the glutamate synthase gene probably happened earlier in evolution and affected a wider range of eukaryotes.     

Advances in livestock nuclear transfer

Cloning and transgenic animal production have been greatly enhanced by the development of nuclear transfer technology. In the past, genetic modification in domestic animals was not tightly controlled. With the nuclear transfer technology one can now create some domestic animals with specific genetic modifications. An ever-expanding variety of cell types have been successfully used as donors to create the clones. Both cell fusion and microinjection are successfully being used to create these animals. However, it is still not clear which stage(s) of the cell cycle for donor and recipient cells yield the greatest degree of development. While for the most part gene expression is reprogrammed in nuclear transfer embryos, all structural changes may not be corrected as evidenced by the length of the telomeres in sheep resulting from nuclear transfer. Even after these animals are created the question of "are they really clones?" arises due to mitochondrial inheritance from the donor cell versus the recipient oocyte. This review discusses these issues as they relate to livestock.     

Nuclear remodeling and reprogramming in transgenic pig production

The manufacture of pigs with modifications to specific chromosomal regions requires that the modification first be made in somatic cells. The modified cells can then be used as donors for nuclear transfer (NT) in an attempt to clone that cell into a newborn animal. Unfortunately the procedures are inefficient and sometimes lead to animals that are abnormal. The cause of these abnormalities is likely established during the first cell cycle after the NT. Either the donor cell was abnormal or the oocyte cytoplasm was unable to adequately remodel the donor nucleus such that it was structured similar to the pronucleus of a zygote. A better understanding of chromatin remodeling and subsequent developmental gene expression will provide clues as to how procedures can be modified to generate fertile animals more efficiently.     

Altered expression of Na+/K+–ATPase and other osmoregulatory genes in the gills of euryhaline animals in response to salinity transfer: A meta-analysis of 59 quantitative PCR studies over 10 years

Recent advances in molecular techniques have allowed gene expression in euryhaline animals to be quantified during salinity transfers. As these investigations transition from studying single genes to utilizing genomics-based methodologies, it is an appropriate time to summarize single gene studies. Therefore, a meta-analysis was performed on 59 published studies that used quantitative polymerase chain reaction (qPCR) to examine expression of osmoregulatory genes (the Na⁺/K⁺–ATPase, NKA; the Na⁺/K⁺/2Cl^? cotransporter, NKCC; carbonic anhydrase, CA; the cystic fibrosis transmembrane regulator, CFTR; and the H⁺–ATPase, HAT) in response to salinity transfer. Based on 887 calculated effect sizes, NKA, NKCC, CA, and HAT are up-regulated after salinity transfer, while surprisingly, CFTR is unchanged. Meta-analysis also identified influential factors contributing to these changes. For example, expression was highest: 1) during transfers from higher to lower salinities comprising a physiological transition from osmoconformity to osmoregulation, 2) 1–3 days following transfer, 3) during dissimilar transfers, and 4) in crustaceans rather than teleosts. Methodological characteristics (e.g., types of controls) were not important. Experiments lacking in the current literature were also identified. Meta-analyses are powerful tools for quantitatively synthesizing a large body of literature, and this report serves as a template for their application in other areas of comparative physiology.     

Where do animal alpha-amylases come from? An interkingdom trip

Alpha-amylases are widely found in eukaryotes and prokaryotes. Few amino acids are conserved among these organisms, but at an intra-kingdom level, conserved protein domains exist. In animals, numerous conserved stretches are considered as typical of animal alpha-amylases. Searching databases, we found no animal-type alpha-amylases outside the Bilateria. Instead, we found in the sponge Reniera sp. and in the sea anemone Nematostella vectensis, alpha-amylases whose most similar cognate was that of the amoeba Dictyostelium discoideum. We found that this "Dictyo-type" alpha-amylase was shared not only by these non-Bilaterian animals, but also by other Amoebozoa, Choanoflagellates, and Fungi. This suggested that the Dictyo-type alpha-amylase was present in the last common ancestor of Unikonts. The additional presence of the Dictyo-type in some Ciliates and Excavates, suggests that horizontal gene transfers may have occurred among Eukaryotes. We have also detected putative interkingdom transfers of amylase genes, which obscured the historical reconstitution. Several alternative scenarii are discussed.     

No evidence for germ-line transmission following prenatal and early postnatal AAV-mediated gene delivery

BACKGROUND: Recombinant adeno-associated viruses have been used successfully in a number of pre-clinical and clinical gene therapy studies. Since there is a broad consensus that gene therapy must not lead to germ-line transmission, the potential of such vectors for inadvertent gene transfer into germ cells deserves special attention. This applies in particular to pre- or perinatal vector application which has been considered for diseases presenting with morbidity already at birth. METHODS: AAV serotype 2 derived vectors carrying a beta-galactosidase reporter gene or human clotting factor IX cDNA were injected intraperitoneally or via a yolk sac vein into mouse fetuses or administered intravascularly to newborn mice. Tissue samples of the treated animals including the gonads as well as sperm DNA, obtained by differential lysis of one testis of each male animal, and the offspring of all treated mice were investigated for the presence of vector DNA by nested PCR. In positive samples, the copy number of the vector was determined by quantitative real-time PCR. RESULTS: AAV vectors administered intraperitoneally or intravascularly to fetal or newborn mice reached the gonads of these animals and persisted there for time periods greater than one year. Intravascular injection of the vector resulted more frequently in gene transfer to the gonads than intraperitoneal injection. Vector copy numbers in the gonads ranged from 0.3 to 74 per 10(4) cell equivalents. However, neither in isolated sperm DNA from the treated animals nor in their offspring were vector sequences detectable. CONCLUSIONS: These data suggest the risk of inadvertent germ-line transmission following prenatal or early postnatal AAV type 2 mediated gene delivery to be very low.     

Efficiency of electron transport processes

Efficiency of electron transport along the linear chain of molecules was investigated from a dynamic viewpoint. It was proposed that two kinds of efficiency are important for electron transport; one is energy efficiency, the other quantum efficiency. In this paper, these two efficiencies are defined for a linear chain system and the correlation between these quantities and the arrangement of various electron transfers is investigated. The optimization of energy and quantum efficiency is found to set different conditions on the arrangement of the rate constants of electron transfer, and there is strong correlation between neighboring electron transfers. In order to maximize both efficiencies, the rate constants of forward and backward transfers of electrons should be bounded by one another in a limited range. In particular, when there are some bypass reactions on the linear chain, as is the case for photosynthesis and respiration, the rate of the backward transfer should be the same order of magnitude as that of the next forward transfer. The present results are applied to some biological processes. In the early stage of photosynthetic electron transfer it seems that quantum efficiency is more important than energy efficiency. The quantum efficiency is close to unity, whereas a considerable part of the free energy is wasted as heat during the primary electron transfers. On the other hand, in the slower electron transfer processes in photosynthesis and respiration, which take place mostly near equilibrium, the energy efficiency seems to be more important than the quantum efficiency. The relation of these properties to biological function is discussed.     

Functional replacement of a primary metabolic pathway via multiple independent eukaryote‐to‐eukaryote gene transfers and selective retention

Although lateral gene transfer (LGT) is now recognized as a major force in the evolution of prokaryotes, the contribution of LGT to the evolution and diversification of eukaryotes is less understood. Notably, transfers of complete pathways are believed to be less likely between eukaryotes, because the successful transfer of a pathway requires the physical clustering of functionally related genes. Here, we report that in one of the closest unicellular relatives of animals, the choanoflagellate, Monosiga, three genes whose products work together in the glutamate synthase cycle are of algal origin. The concerted retention of these three independently acquired genes is best explained as the consequence of a series of adaptive replacement events. More generally, this study argues that (i) eukaryote‐to‐eukaryote transfers of entire metabolic pathways are possible, (ii) adaptive functional replacements of primary pathways can occur, and (iii) functional replacements involving eukaryotic genes are likely to have also contributed to the evolution of eukaryotes. Lastly, these data underscore the potential contribution of algal genes to the evolution of nonphotosynthetic lineages.     

A "chimera" theory on the origin of dicyemid mesozoans: evolution driven by frequent lateral gene transfer from host to parasite

The phylogenetic status of the enigmatic dicyemid mesozoans is still uncertain. Are they primitive multicellular organisms or degenerate triploblastic animals? Presently, the latter view is accepted. A phylogenetic analysis of 18S rDNA sequences placed dicyemids within the animal clade, and this was supported by the discovery of a Hox-type gene with a lophotrochozoan signature sequence. This molecular information suggests that dicyemid mesozoans evolved from an ancestral animal degenerately. Considering their extreme simplicity, which is probably due to parasitism, they might have come from an early embryo via a radical transformation, i.e. neoteny. Irrespective of this molecular information, dicyemid mesozoans retain many protistan-like or extremely primitive features, such as tubular mitochondrial cristae, endocytic ability from the outer surface, and the absence of collagenous tissue, while they do not share noticeable synapomorphy with animals. In addition, the 5S rRNA phylogeny suggests a somewhat closer kinship with protozoan ciliates than with animals. If we accept this clear contradiction, dicyemids should be regarded as a chimera of animals and protistans. Here, we discuss the traditional theory of extreme degeneration via parasitism, and then propose a new "chimera" theory in which dicyemid mesozoans are exposed to a continual flow of genetic information via eating host tissues from the outer surface by endocytosis. Consequently, many of their intrinsic genes have been replaced by host-derived genes through lateral gene transfer (LGT), implying that LGT is a key driving force in the evolution of dicyemid mesozoans.     

Why kin and group selection models may not be enough to explain human other-regarding behaviour

Models of kin or group selection usually feature only one possible fitness transfer. The phenotypes are either to make this transfer or not to make it and for any given fitness transfer, Hamilton's rule predicts which of the two phenotypes will spread. In this article we allow for the possibility that different individuals or different generations face similar, but not necessarily identical possibilities for fitness transfers. In this setting, phenotypes are preference relations, which concisely specify behaviour for a range of possible fitness transfers (rather than being a specification for only one particular situation an animal or human can be in). For this more general set-up, we find that only preference relations that are linear in fitnesses can be explained using models of kin selection and that the same applies to a large class of group selection models. This provides a new implication of hierarchical selection models that could in principle falsify them, even if relatedness--or a parameter for assortativeness--is unknown. The empirical evidence for humans suggests that hierarchical selection models alone are not enough to explain their other-regarding or altruistic behaviour.     

Evidence for the presence of a cellulase gene in the last common ancestor of bilaterian animals

Until recently, the textbook view of cellulose hydrolysis in animals was that gut-resident symbiotic organisms such as bacteria or unicellular eukaryotes are responsible for the cellulases produced. This view has been challenged by the characterization and sequencing of endogenous cellulase genes from some invertebrate animals, including plant-parasitic nematodes, arthropods and a mollusc. Most of these genes are completely unrelated in terms of sequence, and their evolutionary origins remain unclear. In the case of plant-parasitic nematodes, it has been suggested that their ancestor obtained a cellulase gene via horizontal gene transfer from a prokaryote, and similar suggestions have been made about a cellulase gene recently discovered in a sea squirt. To improve understanding about the evolution of animal cellulases, we searched for all known types of these enzymes in GenBank, and performed phylogenetic comparisons. Low phylogenetic resolution was found among most of the sequences examined, however, positional identity in the introns of cellulase genes from a termite, a sea squirt and an abalone provided compelling evidence that a similar gene was present in the last common ancestor of protostomes and deuterostomes. In a different enzyme family, cellulases from beetles and plant-parasitic nematodes were found to cluster together. This result questions the idea of lateral gene transfer into the ancestors of the latter, although statistical tests did not allow this possibility to be ruled out. Overall, our results suggest that at least one family of endogenous cellulases may be more widespread in animals than previously thought.     

Socially transferred materials: why and how to study them

When biological material is transferred from one individual’s body to another, as in ejaculate, eggs, and milk, secondary donor-produced molecules are often transferred along with the main cargo, and influence the physiology and fitness of the receiver. Both social and solitary animals exhibit such social transfers at certain life stages. The secondary, bioactive, and transfer-supporting components in socially transferred materials have evolved convergently to the point where they are used in applications across taxa and type of transfer. The composition of these materials is typically highly dynamic and context dependent, and their components drive the physiological and behavioral evolution of many taxa. Our establishment of the concept of socially transferred materials unifies this multidisciplinary topic and will benefit both theory and applications.