scholarly journals Contribution of Lateral Gene Transfer to the evolution of the eukaryotic fungus Piromyces sp. E2: Massive bacterial transfer of genes involved in carbohydrate metabolism

2019 ◽  
Author(s):  
Isabel Duarte ◽  
Martijn A. Huynen

ABSTRACTLateral gene transfer (also known as Horizontal Gene Transfer) is the transmission of genetic material between phylogenetically unrelated organisms. Previous studies have been showing the importance of this process for the evolution of unicellular eukaryotes, particularly those living in highly competitive niches such as the herbivore gut.Pyromices sp. is an obligate anaerobic chytrid fungus that grows as a commensal organism in the gut of mammalian herbivores, possessing hydrogenosomes instead of mitochondria, producing hydrogen, and playing a key role in the digestion of plant cell wall material. These particular features make its genome particularly valuable for the study of the evolution and adaptation of unicellular eukaryotes to the cellulose-rich and anaerobic environment of the herbivore gut.Here we performed a detailed large-scale lateral gene transfer (LGT) analysis of the genome from the chytrid fungus Piromyces sp. strain E2. For this we set out to elucidate (i) which proteins were likely transferred to its genome, (ii) from which bacterial donor species, and (iii) which functions were laterally acquired. Using sequence comparison and phylogenetic analyses, we have found 704 LGT candidates, representing nearly 5% of the Piromyces sp. orfeome (i.e. the complete set of open reading frames), mostly transferred from Firmicutes, Fibrobacteres, Bacteroidetes and Proteobacteria, closely following the microbial abundance reported for the herbivore gut. With respect to the functional analysis, the LGT candidate set includes proteins from 250 different orthologous groups, with a clear over-representation of genes belonging to the Carbohydrate Transport and Metabolism functional class. Finally, we performed a graph density analysis on the metabolic pathways formed by the LGT candidate proteins, showing that the acquired functions fit cohesively within Piromyces metabolic network, and are not randomly distributed within the global KEGG metabolic map. Overall, our study suggests that Piromyces’ adaptation to living anaerobically and in the a cellulose-rich environment has been undoubtedly fostered by the acquisition of foreign genes from bacterial neighbors, showing the global importance of such evolutionary mechanisms for successful eukaryotic thriving in such competitive environments.

2020 ◽  
Author(s):  
Andy O. Leu ◽  
Simon J. McIlroy ◽  
Jun Ye ◽  
Donovan H. Parks ◽  
Victoria J. Orphan ◽  
...  

AbstractAnaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceace metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate, and the reduction of arsenate, selenate and elemental sulfur. Numerous membrane-bound multi-heme c type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humics and syntrophic partners.ImportanceAOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance to the global carbon cycle and climate change modelling. While the oxidation of methane coupled to sulphate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae as they are absent in related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles.


2021 ◽  
Author(s):  
Apurva Narechania ◽  
Rob DeSalle ◽  
Barun Mathema ◽  
Barry N Kreiswirth ◽  
Paul J Planet

Most microbes have the capacity to acquire genetic material from their environment. Recombination of foreign DNA yields genomes that are, at least in part, incongruent with the vertical history of their species. Dominant approaches for detecting such horizontal gene transfer (HGT) and recombination are phylogenetic, requiring a painstaking series of analyses including sequence-based clustering, alignment, and phylogenetic tree reconstruction. Given the breakneck pace of genome sequencing, these traditional pan-genomic methods do not scale. Here we propose an alignment-free and tree-free technique based on the sequential information bottleneck (SIB), an optimization procedure designed to extract some portion of relevant information from one random variable conditioned on another. In our case, this joint probability distribution tabulates occurrence counts of k-mers with respect to their genomes of origin (the relevance information) with the expectation that HGT and recombination will create a strong signal that distinguishes certain sets of co-occuring k-mers. The technique is conceptualized as a rate-distortion problem. We measure distortion in the relevance information as k-mers are compressed into clusters based on their co-occurrence in the source genomes. This approach is similar to topic mining in the Natural Language Processing (NLP) literature. The result is model-free, unsupervised compression of k-mers into genomic topics that trace tracts of shared genome sequence whether vertically or horizontally acquired. We examine the performance of SIB on simulated data and on the known large-scale recombination event that formed the Staphylococcus aureus ST239 clade. We use this technique to detect recombined regions and recover the vertically inherited core genome with a fraction of the computing power required of current phylogenetic methods.


2013 ◽  
Vol 280 (1763) ◽  
pp. 20131021 ◽  
Author(s):  
Yannick Pauchet ◽  
David G. Heckel

The primary plant cell wall comprises the most abundant polysaccharides on the Earth and represents a rich source of energy for organisms which have evolved the ability to digest them. Enzymes able to degrade plant cell wall polysaccharides are widely distributed in micro-organisms but are generally absent in animals, although their presence in insects, especially phytophagous beetles from the superfamilies Chrysomeloidea and Curculionoidea, has recently begun to be appreciated. The observed patchy distribution of endogenous genes encoding these enzymes in animals has raised questions about their evolutionary origins. Recent evidence suggests that endogenous plant cell wall degrading enzymes-encoding genes have been acquired by animals through a mechanism known as horizontal gene transfer (HGT). HGT describes how genetic material is moved by means other than vertical inheritance from a parent to an offspring. Here, we provide evidence that the mustard leaf beetle, Phaedon cochleariae , possesses in its genome genes encoding active xylanases from the glycoside hydrolase family 11 (GH11). We also provide evidence that these genes were originally acquired by P. cochleariae from a species of gammaproteobacteria through HGT. This represents the first example of the presence of genes from the GH11 family in animals.


2008 ◽  
Vol 363 (1505) ◽  
pp. 2813-2820 ◽  
Author(s):  
Michael L Arnold ◽  
Yuval Sapir ◽  
Noland H Martin

Data supporting the occurrence of adaptive trait transfer (i.e. the transfer of genes and thus the phenotype of an adaptive trait through viral recombination, lateral gene transfer or introgressive hybridization) are provided in this review. Specifically, we discuss examples of lateral gene transfer and introgressive hybridization that have resulted in the transfer or de novo origin of adaptations. The evolutionary clades in which this process has been identified include all types of organisms. However, we restrict our discussion to bacteria, fungi, plants and animals. Each of these examples reflects the same consequence, namely that the transfer of genetic material, through whatever mechanism, may result in adaptive evolution. In particular, each of the events discussed has been inferred to impact adaptations to novel environmental settings in the recipient lineage.


2010 ◽  
Vol 3 (1) ◽  
pp. 85-92 ◽  
Author(s):  
Maja Velhner ◽  
Jelena Petrović ◽  
Igor Stojanov ◽  
Radomir Ratajac ◽  
Dragica Stojanović

Wide application of antimicorbial agents forces bacteria to utilize specific genes and rearrange genomic structure in order to survive in the environment. In this article lateral gene transfer, mobile genetic elements, plasmid mediated resistance and spontaneous mutators in bacteria are briefly described. This resourceful means, by which microorganisms manage to communicate and transfer genetic material in their own kingdom, raises concerns about the possibility to keep microbial infections under control in the future.


mBio ◽  
2020 ◽  
Vol 11 (3) ◽  
Author(s):  
Andy O. Leu ◽  
Simon J. McIlroy ◽  
Jun Ye ◽  
Donovan H. Parks ◽  
Victoria J. Orphan ◽  
...  

ABSTRACT Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceae metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate and the reduction of arsenate, selenate, and elemental sulfur. Numerous membrane-bound multiheme c-type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humic substances, and syntrophic partners. IMPORTANCE AOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance for the global carbon cycle and climate change modeling. While the oxidation of methane coupled to sulfate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study, we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae, as they are absent from related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles.


2019 ◽  
Vol 37 (3) ◽  
pp. 651-659 ◽  
Author(s):  
Naoji Yubuki ◽  
Luis Javier Galindo ◽  
Guillaume Reboul ◽  
Purificación López-García ◽  
Matthew W Brown ◽  
...  

Abstract Lateral gene transfer is a very common process in bacterial and archaeal evolution, playing an important role in the adaptation to new environments. In eukaryotes, its role and frequency remain highly debated, although recent research supports that gene transfer from bacteria to diverse eukaryotes may be much more common than previously appreciated. However, most of this research focused on animals and the true phylogenetic and functional impact of bacterial genes in less-studied microbial eukaryotic groups remains largely unknown. Here, we have analyzed transcriptome data from the deep-branching stramenopile Opalinidae, common members of frog gut microbiomes, and distantly related to the well-known genus Blastocystis. Phylogenetic analyses suggest the early acquisition of several bacterial genes in a common ancestor of both lineages. Those lateral gene transfers most likely facilitated the adaptation of the free-living ancestor of the Opalinidae–Blastocystis symbiotic group to new niches in the oxygen-depleted animal gut environment.


2020 ◽  
Author(s):  
Marco Colnaghi ◽  
Nick Lane ◽  
Andrew Pomiankowski

ABSTRACTProkaryotes generally reproduce clonally but can also acquire new genetic material via lateral gene transfer (LGT). Like sex, LGT can prevent the accumulation of deleterious mutations predicted by Muller’s ratchet for asexual populations. This similarity between sex and LGT raises the question why did eukaryotes abandon LGT in favor of sexual reproduction? Understanding the limitations of LGT provides insight into this evolutionary transition. We model the evolution of a haploid population undergoing LGT at a rate λ and subjected to a mutation rate μ. We take into account recombination length, L, and genome size, g, neglected by previous theoretical models. We confirm that LGT counters Muller’s ratchet by reducing the rate of fixation of deleterious mutations in small genomes. We then demonstrate that this beneficial effect declines rapidly with genome size. Populations with larger genomes are subjected to a faster rate of fixation of deleterious mutations and become more vulnerable to stochastic frequency fluctuations. Muller’s ratchet therefore generates a strong constraint on genome size. Importantly, we show that the degeneration of larger genomes can be resisted by increases in the recombination length, the average number of contiguous genes drawn from the environment for LGT. Large increases in genome size, as in early eukaryotes, are only possible as L reaches the same order of magnitude as g. This requirement for recombination across the whole genome can explain the strong selective pressure towards the evolution of sexual cell fusion and reciprocal recombination during early eukaryotic evolution – the origin of meiotic sex.


Mobile DNA ◽  
2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Izabella L. Tambones ◽  
Annabelle Haudry ◽  
Maryanna C. Simão ◽  
Claudia M. A. Carareto

Abstract Background The use of large-scale genomic analyses has resulted in an improvement of transposable element sampling and a significant increase in the number of reported HTT (horizontal transfer of transposable elements) events by expanding the sampling of transposable element sequences in general and of specific families of these elements in particular, which were previously poorly sampled. In this study, we investigated the occurrence of HTT events in a group of elements that, until recently, were uncommon among the HTT records in Drosophila – the Jockey elements, members of the LINE (long interspersed nuclear element) order of non-LTR (long terminal repeat) retrotransposons. The sequences of 111 Jockey families deposited in Repbase that met the criteria of the analysis were used to identify Jockey sequences in 48 genomes of Drosophilidae (genus Drosophila, subgenus Sophophora: melanogaster, obscura and willistoni groups; subgenus Drosophila: immigrans, melanica, repleta, robusta, virilis and grimshawi groups; subgenus Dorsilopha: busckii group; genus/subgenus Zaprionus and genus Scaptodrosophila). Results Phylogenetic analyses revealed 72 Jockey families in 41 genomes. Combined analyses revealed 15 potential HTT events between species belonging to different genera and species groups of Drosophilidae, providing evidence for the flow of genetic material favoured by the spatio-temporal sharing of these species present in the Palaeartic or Afrotropical region. Conclusions Our results provide phylogenetic, biogeographic and temporal evidence of horizontal transfers of the Jockey elements, increase the number of rare records of HTT in specific families of LINE elements, increase the number of known occurrences of these events, and enable a broad understanding of the evolutionary dynamics of these elements and the host species.


Information ◽  
2020 ◽  
Vol 11 (7) ◽  
pp. 352
Author(s):  
Nathalie Gontier

Variation, adaptation, heredity and fitness, constraints and affordances, speciation, and extinction form the building blocks of the (Neo-)Darwinian research program, and several of these have been called “Darwinian principles”. Here, we suggest that caution should be taken in calling these principles Darwinian because of the important role played by reticulate evolutionary mechanisms and processes in also bringing about these phenomena. Reticulate mechanisms and processes include symbiosis, symbiogenesis, lateral gene transfer, infective heredity mediated by genetic and organismal mobility, and hybridization. Because the “Darwinian principles” are brought about by both vertical and reticulate evolutionary mechanisms and processes, they should be understood as foundational for a more pluralistic theory of evolution, one that surpasses the classic scope of the Modern and the Neo-Darwinian Synthesis. Reticulate evolution moreover demonstrates that what conventional (Neo-)Darwinian theories treat as intra-species features of evolution frequently involve reticulate interactions between organisms from very different taxonomic categories. Variation, adaptation, heredity and fitness, constraints and affordances, speciation, and extinction therefore cannot be understood as “traits” or “properties” of genes, organisms, species, or ecosystems because the phenomena are irreducible to specific units and levels of an evolutionary hierarchy. Instead, these general principles of evolution need to be understood as common goods that come about through interactions between different units and levels of evolutionary hierarchies, and they are exherent rather than inherent properties of individuals.


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