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Evolutionary Genetics of Microbial Symbiosis
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Evolutionary Genetics of Microbial Symbiosis

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Population and Evolutionary Genetics and Genomics".

Deadline for manuscript submissions: closed (15 June 2020) | Viewed by 30149

Special Issue Editors

Prof. Laura Baldo

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Guest Editor
Department of Evolutionary Biology, Ecology and Environmental Sciences, University of Barcelona, Barcelona, Spain
Interests: symbiosis; evolutionary ecology; metagenomics; gut microbiota
Prof. Jack Werren

E-Mail Website
Guest Editor
Department of Biology, University of Rochester, Rochester, NY, USA
Interests: endosymbionts; evolution of inherited microorganisms; genetic basis of morphological and behavioral differences between species; genetic conflict and the evolution of "parasitic" or "selfish" DNA

Special Issue Information

Dear Colleagues,

Symbiosis is defined as the physical and persistent interactions among unlike organisms and has led to the emergence of remarkable novelties in the course of evolution (e.g., the appearance of organelles). Symbiosis currently underpins the success of some of the most important ecosystems in nature (e.g., coral reefs). Microbial symbioses, in particular, are now seen as intrinsically embedded in all multicellular organisms, where they can contribute to phenotypic diversity across biological levels of organization (from molecular to ecosystem traits), ultimately affecting the co-evolution of life. Recent molecular advances in the study of microbial diversity have begun to reveal the range in complexity and number of players of microbial symbiotic systems, from stable and highly specific single host-bacteria associations (e.g., Buchnera in aphids) to widespread communities of microbes establishing dynamic interactions between each other and with their hosts (e.g., the animal gut microbiota). Host and microbes can engage in extensive cross-kingdom molecular dialogue that we have only begun to disentangle. Not only do physically associated organisms “communicate”, they can also integrate information, complement metabolic pathways, and even exchange their DNA, in some cases becoming sufficiently integrated to possibly become a higher evolutionary unit of selection. This extensive interplay among microbes and hosts has enormous implications in the emergence of novel traits and the overall diversification of life.

In this Special Issue, we invite reviews, prospectives, and research papers that contribute to our understanding of the evolutionary impact of microbial symbioses. Specifically, we would like to target the following: the genetic factors shaping spatial and temporal dynamics in host–microbial communities; the role of microbial symbiosis in organismal adaptation and evolution; the concept of genomic individuality in symbiotic systems; the genetic bases of the symbiotic–host and symbiont–symbiont interaction; the phylogenomic and genomic (co)evolution of symbionts and hosts; the modes of transmission, acquisition, and association of microbe–host systems; and new methodologies and approaches to disentangle the genetic interchange among symbionts (including single-cell genomics). Manuscripts can target both highly specific host–symbiont interactions (e.g., endosymbionts), as well as microbial communities (bacterial, viral, fungal, and protist) residing in animals and plants. We welcome studies on new symbiotic models.

Prof. Laura Baldo
Prof. Jack Werren
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Genes is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • host-associated microbial communities
  • endosymbionts
  • genetics of symbiosis
  • genetic interactions among host–microbes

Published Papers (8 papers)

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Editorial

Jump to: Research, Review

3 pages, 181 KiB  
Editorial
Evolutionary Genetics of Microbial Symbiosis
by Laura Baldo and John H. Werren
Genes 2021, 12(3), 327; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12030327 - 25 Feb 2021
Cited by 3 | Viewed by 1461
Abstract
Symbiosis is the living together of dissimilar organisms [...] Full article
(This article belongs to the Special Issue Evolutionary Genetics of Microbial Symbiosis)

Research

Jump to: Editorial, Review

21 pages, 3437 KiB  
Article
Genomic Comparison of Insect Gut Symbionts from Divergent Burkholderia Subclades
by Kazutaka Takeshita and Yoshitomo Kikuchi
Genes 2020, 11(7), 744; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11070744 - 03 Jul 2020
Cited by 10 | Viewed by 3900
Abstract
Stink bugs of the superfamilies Coreoidea and Lygaeoidea establish gut symbioses with environmentally acquired bacteria of the genus Burkholderia sensu lato. In the genus Burkholderia, the stink bug-associated strains form a monophyletic clade, named stink bug-associated beneficial and environmental (SBE) clade (or [...] Read more.
Stink bugs of the superfamilies Coreoidea and Lygaeoidea establish gut symbioses with environmentally acquired bacteria of the genus Burkholderia sensu lato. In the genus Burkholderia, the stink bug-associated strains form a monophyletic clade, named stink bug-associated beneficial and environmental (SBE) clade (or Caballeronia). Recently, we revealed that members of the family Largidae of the superfamily Pyrrhocoroidea are associated with Burkholderia but not specifically with the SBE Burkholderia; largid bugs harbor symbionts that belong to a clade of plant-associated group of Burkholderia, called plant-associated beneficial and environmental (PBE) clade (or Paraburkholderia). To understand the genomic features of Burkholderia symbionts of stink bugs, we isolated two symbiotic Burkholderia strains from a bordered plant bug Physopellta gutta (Pyrrhocoroidea: Largidae) and determined their complete genomes. The genome sizes of the insect-associated PBE (iPBE) are 9.5 Mb and 11.2 Mb, both of which are larger than the genomes of the SBE Burkholderia symbionts. A whole-genome comparison between two iPBE symbionts and three SBE symbionts highlighted that all previously reported symbiosis factors are shared and that 282 genes are specifically conserved in the five stink bug symbionts, over one-third of which have unknown function. Among the symbiont-specific genes, about 40 genes formed a cluster in all five symbionts; this suggests a “symbiotic island” in the genome of stink bug-associated Burkholderia. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Microbial Symbiosis)
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18 pages, 3078 KiB  
Article
Paraburkholderia Symbionts Display Variable Infection Patterns That Are Not Predictive of Amoeba Host Outcomes
by Jacob W. Miller, Colleen R. Bocke, Andrew R. Tresslar, Emily M. Schniepp and Susanne DiSalvo
Genes 2020, 11(6), 674; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11060674 - 20 Jun 2020
Cited by 9 | Viewed by 3023
Abstract
Symbiotic interactions exist within a parasitism to mutualism continuum that is influenced, among others, by genes and context. Dynamics of intracellular invasion, replication, and prevalence may underscore both host survivability and symbiont stability. More infectious symbionts might exert higher corresponding costs to hosts, [...] Read more.
Symbiotic interactions exist within a parasitism to mutualism continuum that is influenced, among others, by genes and context. Dynamics of intracellular invasion, replication, and prevalence may underscore both host survivability and symbiont stability. More infectious symbionts might exert higher corresponding costs to hosts, which could ultimately disadvantage both partners. Here, we quantify infection patterns of diverse Paraburkholderia symbiont genotypes in their amoeba host Dictyostelium discoideum and probe the relationship between these patterns and host outcomes. We exposed D. discoideum to thirteen strains of Paraburkholderia each belonging to one of the three symbiont species found to naturally infect D. discoideum: Paraburkholderia agricolaris, Paraburkholderia hayleyella, and Paraburkholderia bonniea. We quantified the infection prevalence and intracellular density of fluorescently labeled symbionts along with the final host population size using flow cytometry and confocal microscopy. We find that infection phenotypes vary across symbiont strains. Symbionts belonging to the same species generally display similar infection patterns but are interestingly distinct when it comes to host outcomes. This results in final infection loads that do not strongly correlate to final host outcomes, suggesting other genetic factors that are not a direct cause or consequence of symbiont abundance impact host fitness. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Microbial Symbiosis)
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17 pages, 3037 KiB  
Article
Rhizobia Isolated from the Relict Legume Vavilovia formosa Represent a Genetically Specific Group within Rhizobium leguminosarum biovar viciae
by Anastasiia K. Kimeklis, Elizaveta R. Chirak, Irina G. Kuznetsova, Anna L. Sazanova, Vera I. Safronova, Andrey A. Belimov, Olga P. Onishchuk, Oksana N. Kurchak, Tatyana S. Aksenova, Alexander G. Pinaev, Evgeny E. Andronov and Nikolay A. Provorov
Genes 2019, 10(12), 991; https://0-doi-org.brum.beds.ac.uk/10.3390/genes10120991 - 01 Dec 2019
Cited by 10 | Viewed by 2431
Abstract
Twenty-two rhizobia strains isolated from three distinct populations (North Ossetia, Dagestan, and Armenia) of a relict legume Vavilovia formosa were analysed to determine their position within Rhizobium leguminosarum biovar viciae (Rlv). These bacteria are described as symbionts of four plant genera [...] Read more.
Twenty-two rhizobia strains isolated from three distinct populations (North Ossetia, Dagestan, and Armenia) of a relict legume Vavilovia formosa were analysed to determine their position within Rhizobium leguminosarum biovar viciae (Rlv). These bacteria are described as symbionts of four plant genera Pisum, Vicia, Lathyrus, and Lens from the Fabeae tribe, of which Vavilovia is considered to be closest to its last common ancestor (LCA). In contrast to biovar viciae, bacteria from Rhizobium leguminosarum biovar trifolii (Rlt) inoculate plants from the Trifolieae tribe. Comparison of house-keeping (hkg: 16S rRNA, glnII, gltA, and dnaK) and symbiotic (sym: nodA, nodC, nodD, and nifH) genes of the symbionts of V. formosa with those of other Rlv and Rlt strains reveals a significant group separation, which was most pronounced for sym genes. A remarkable feature of the strains isolated from V. formosa was the presence of the nodX gene, which was commonly found in Rlv strains isolated from Afghanistan pea genotypes. Tube testing of different strains on nine plant species, including all genera from the Fabeae tribe, demonstrated that the strains from V. formosa nodulated the same cross inoculation group as the other Rlv strains. Comparison of nucleotide similarity in sym genes suggested that their diversification within sym-biotypes of Rlv was elicited by host plants. Contrariwise, that of hkg genes could be caused by either local adaptation to soil niches or by genetic drift. Long-term ecological isolation, genetic separation, and the ancestral position of V. formosa suggested that symbionts of V. formosa could be responsible for preserving ancestral genotypes of the Rlv biovar. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Microbial Symbiosis)
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20 pages, 2082 KiB  
Article
Search for Ancestral Features in Genomes of Rhizobium leguminosarum bv. viciae Strains Isolated from the Relict Legume Vavilovia formosa
by Elizaveta R. Chirak, Anastasiia K. Kimeklis, Evgenii S. Karasev, Vladimir V. Kopat, Vera I. Safronova, Andrey A. Belimov, Tatiana S. Aksenova, Marsel R. Kabilov, Nikolay A. Provorov and Evgeny E. Andronov
Genes 2019, 10(12), 990; https://0-doi-org.brum.beds.ac.uk/10.3390/genes10120990 - 01 Dec 2019
Cited by 8 | Viewed by 2484
Abstract
Vavilovia formosa is a relict leguminous plant growing in hard-to-reach habitats in the rocky highlands of the Caucasus and Middle East, and it is considered as the putative closest living relative of the last common ancestor (LCA) of the Fabeae tribe. Symbionts of [...] Read more.
Vavilovia formosa is a relict leguminous plant growing in hard-to-reach habitats in the rocky highlands of the Caucasus and Middle East, and it is considered as the putative closest living relative of the last common ancestor (LCA) of the Fabeae tribe. Symbionts of Vavilovia belonging to Rhizobium leguminosarum bv. viciae compose a discrete group that differs from the other strains, especially in the nucleotide sequences of the symbiotically specialised (sym) genes. Comparison of the genomes of Vavilovia strains with the reference group composed of R. leguminosarum bv. viciae strains isolated from Pisum and Vicia demonstrated that the vavilovia strains have a set of genomic features, probably indicating the important stages of microevolution of the symbiotic system. Specifically, symbionts of Vavilovia (considered as an ancestral group) demonstrated a scattered arrangement of sym genes (>90 kb cluster on pSym), with the location of nodT gene outside of the other nod operons, the presence of nodX and fixW, and the absence of chromosomal fixNOPQ copies. In contrast, the reference (derived) group harboured sym genes as a compact cluster (<60 kb) on a single pSym, lacking nodX and fixW, with nodT between nodN and nodO, and possessing chromosomal fixNOPQ copies. The TOM strain, obtained from nodules of the primitive “Afghan” peas, occupied an intermediate position because it has the chromosomal fixNOPQ copy, while the other features, the most important of which is presence of nodX and fixW, were similar to the Vavilovia strains. We suggest that genome evolution from the ancestral to the derived R. leguminosarum bv. viciae groups follows the “gain-and-loss of sym genes” and the “compaction of sym cluster” strategies, which are common for the macro-evolutionary and micro-evolutionary processes. The revealed genomic features are in concordance with a relict status of the vavilovia strains, indicating that V. formosa coexists with ancestral microsymbionts, which are presumably close to the LCA of R. leguminosarum bv. viciae. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Microbial Symbiosis)
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Review

Jump to: Editorial, Research

33 pages, 3344 KiB  
Review
Rediscovering a Forgotten System of Symbiosis: Historical Perspective and Future Potential
by Vincent G. Martinson
Genes 2020, 11(9), 1063; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11091063 - 09 Sep 2020
Cited by 13 | Viewed by 6456
Abstract
While the majority of symbiosis research is focused on bacteria, microbial eukaryotes play important roles in the microbiota and as pathogens, especially the incredibly diverse Fungi kingdom. The recent emergence of widespread pathogens in wildlife (bats, amphibians, snakes) and multidrug-resistant opportunists in human [...] Read more.
While the majority of symbiosis research is focused on bacteria, microbial eukaryotes play important roles in the microbiota and as pathogens, especially the incredibly diverse Fungi kingdom. The recent emergence of widespread pathogens in wildlife (bats, amphibians, snakes) and multidrug-resistant opportunists in human populations (Candida auris) has highlighted the importance of better understanding animal–fungus interactions. Regardless of their prominence there are few animal–fungus symbiosis models, but modern technological advances are allowing researchers to utilize novel organisms and systems. Here, I review a forgotten system of animal–fungus interactions: the beetle–fungus symbioses of Drugstore and Cigarette beetles with their symbiont Symbiotaphrina. As pioneering systems for the study of mutualistic symbioses, they were heavily researched between 1920 and 1970, but have received only sporadic attention in the past 40 years. Several features make them unique research organisms, including (1) the symbiont is both extracellular and intracellular during the life cycle of the host, and (2) both beetle and fungus can be cultured in isolation. Specifically, fungal symbionts intracellularly infect cells in the larval and adult beetle gut, while accessory glands in adult females harbor extracellular fungi. In this way, research on the microbiota, pathogenesis/infection, and mutualism can be performed. Furthermore, these beetles are economically important stored-product pests found worldwide. In addition to providing a historical perspective of the research undertaken and an overview of beetle biology and their symbiosis with Symbiotaphrina, I performed two analyses on publicly available genomic data. First, in a preliminary comparative genomic analysis of the fungal symbionts, I found striking differences in the pathways for the biosynthesis of two B vitamins important for the host beetle, thiamine and biotin. Second, I estimated the most recent common ancestor for Drugstore and Cigarette beetles at 8.8–13.5 Mya using sequence divergence (CO1 gene). Together, these analyses demonstrate that modern methods and data (genomics, transcriptomes, etc.) have great potential to transform these beetle–fungus systems into model systems again. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Microbial Symbiosis)
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22 pages, 1329 KiB  
Review
The Biochemistry of Cytoplasmic Incompatibility Caused by Endosymbiotic Bacteria
by Hongli Chen, Mengwen Zhang and Mark Hochstrasser
Genes 2020, 11(8), 852; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11080852 - 25 Jul 2020
Cited by 29 | Viewed by 5392
Abstract
Many species of arthropods carry maternally inherited bacterial endosymbionts that can influence host sexual reproduction to benefit the bacterium. The most well-known of such reproductive parasites is Wolbachia pipientis. Wolbachia are obligate intracellular α-proteobacteria found in nearly half of all arthropod species. [...] Read more.
Many species of arthropods carry maternally inherited bacterial endosymbionts that can influence host sexual reproduction to benefit the bacterium. The most well-known of such reproductive parasites is Wolbachia pipientis. Wolbachia are obligate intracellular α-proteobacteria found in nearly half of all arthropod species. This success has been attributed in part to their ability to manipulate host reproduction to favor infected females. Cytoplasmic incompatibility (CI), a phenomenon wherein Wolbachia infection renders males sterile when they mate with uninfected females, but not infected females (the rescue mating), appears to be the most common. CI provides a reproductive advantage to infected females in the presence of a threshold level of infected males. The molecular mechanisms of CI and other reproductive manipulations, such as male killing, parthenogenesis, and feminization, have remained mysterious for many decades. It had been proposed by Werren more than two decades ago that CI is caused by a Wolbachia-mediated sperm modification and that rescue is achieved by a Wolbachia-encoded rescue factor in the infected egg. In the past few years, new research has highlighted a set of syntenic Wolbachia gene pairs encoding CI-inducing factors (Cifs) as the key players for the induction of CI and its rescue. Within each Cif pair, the protein encoded by the upstream gene is denoted A and the downstream gene B. To date, two types of Cifs have been characterized based on the enzymatic activity identified in the B protein of each protein pair; one type encodes a deubiquitylase (thus named CI-inducing deubiquitylase or cid), and a second type encodes a nuclease (named CI-inducing nuclease or cin). The CidA and CinA proteins bind tightly and specifically to their respective CidB and CinB partners. In transgenic Drosophila melanogaster, the expression of either the Cid or Cin protein pair in the male germline induces CI and the expression of the cognate A protein in females is sufficient for rescue. With the identity of the Wolbachia CI induction and rescue factors now known, research in the field has turned to directed studies on the molecular mechanisms of CI, which we review here. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Microbial Symbiosis)
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21 pages, 2466 KiB  
Review
Sensing, Signaling, and Secretion: A Review and Analysis of Systems for Regulating Host Interaction in Wolbachia
by Amelia R. I. Lindsey
Genes 2020, 11(7), 813; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11070813 - 16 Jul 2020
Cited by 15 | Viewed by 4158
Abstract
Wolbachia (Anaplasmataceae) is an endosymbiont of arthropods and nematodes that resides within host cells and is well known for manipulating host biology to facilitate transmission via the female germline. The effects Wolbachia has on host physiology, combined with reproductive manipulations, make this bacterium [...] Read more.
Wolbachia (Anaplasmataceae) is an endosymbiont of arthropods and nematodes that resides within host cells and is well known for manipulating host biology to facilitate transmission via the female germline. The effects Wolbachia has on host physiology, combined with reproductive manipulations, make this bacterium a promising candidate for use in biological- and vector-control. While it is becoming increasingly clear that Wolbachia’s effects on host biology are numerous and vary according to the host and the environment, we know very little about the molecular mechanisms behind Wolbachia’s interactions with its host. Here, I analyze 29 Wolbachia genomes for the presence of systems that are likely central to the ability of Wolbachia to respond to and interface with its host, including proteins for sensing, signaling, gene regulation, and secretion. Second, I review conditions under which Wolbachia alters gene expression in response to changes in its environment and discuss other instances where we might hypothesize Wolbachia to regulate gene expression. Findings will direct mechanistic investigations into gene regulation and host-interaction that will deepen our understanding of intracellular infections and enhance applied management efforts that leverage Wolbachia. Full article
(This article belongs to the Special Issue Evolutionary Genetics of Microbial Symbiosis)
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