DOCSLIB.ORG

A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug The All-Rounder Sodalis: A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug Henestaris halophilus (Heteroptera: Henestarinae) and a Critical Examination of Its Evolution Diego Santos-Garcia, Francisco Silva, Shai Morin, Konrad Dettner, Stefan Martin Kuechler To cite this version: Diego Santos-Garcia, Francisco Silva, Shai Morin, Konrad Dettner, Stefan Martin Kuechler. The All-Rounder Sodalis: A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug Henes- taris halophilus (Heteroptera: Henestarinae) and a Critical Examination of Its Evolution. Genome Biology and Evolution, Society for Molecular Biology and Evolution, 2017, 9 (10), pp.2893-2910. 10.1093/gbe/evx202. hal-03270194 HAL Id: hal-03270194 https://hal.archives-ouvertes.fr/hal-03270194 Submitted on 24 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. GBE The All-Rounder Sodalis: A New Bacteriome-Associated Endosymbiont of the Lygaeoid Bug Henestaris halophilus (Heteroptera: Henestarinae) and a Critical Examination of Its Evolution Diego Santos-Garcia1,*, Francisco J. Silva2,3, Shai Morin1, Konrad Dettner4, and Stefan Martin Kuechler4,* 1Department of Entomology, The Hebrew University of Jerusalem, Rehovot, Israel 2Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de Vale` ncia, Spain 3Institute for Integrative Systems Biology (I2SysBio), Universitat de Vale` ncia-CSIC, Spain 4Department of Animal Ecology II, University of Bayreuth, Germany *Corresponding authors: E-mail: [email protected]; [email protected]. Accepted: September 25, 2017 Data deposition: This project has been deposited at ENA of EMBL-EBI under the accession number PRJEB12882. Abstract Hemipteran insects are well-known in their ability to establish symbiotic relationships with bacteria. Among them, heteropteran insects present an array of symbiotic systems, ranging from the most common gut crypt symbiosis to the more restricted bacteriome-associated endosymbiosis, which have only been detected in members of the superfamily Lygaeoidea and the family Cimicidae so far. Genomic data of heteropteran endosymbionts are scarce and have merely been analyzed from the Wolbachia endosymbiont in bed bug and a few gut crypt-associated symbionts in pentatomoid bugs. In this study, we present the first detailed genomic analysis of a bacteriome-associated endosymbiont of a phytophagous heteropteran, present in the seed bug Henestaris halophilus (Hemiptera: Heteroptera: Lygaeoidea). Using phylogenomics and genomics approaches, we have assigned the newly characterized endosymbiont to the Sodalis genus, named as Candidatus Sodalis baculum sp. nov. strain kilmister. In addition, our findings support the reunification of the Sodalis genus, currently divided into six different genera. We have also conducted comparative analyses between 15 Sodalis species that present different genome sizes and symbiotic relationships. These analyses suggest that Ca. Sodalis baculum is a mutualistic endosymbiont capable of supplying the amino acids tyrosine, lysine, and some cofactors to its host. It has a small genome with pseudogenes but no mobile elements, which indicates middle-stage reductive evolution. Most of the genes in Ca. Sodalis baculum are likely to be evolving under purifying selection with several signals pointing to the retention of the lysine/tyrosine biosynthetic pathways compared with other Sodalis. Key words: Lygaeoidea, endosymbiosis, taxonomy, comparative genomics, metabolism, molecular evolution. Introduction organ-like termed bacteriome (Buchner 1965). These intracel- Most insects have established specific associations with bac- lular symbionts (hereafter endosymbionts) are usually defined terial symbionts. These associations show a broad range of as primary, or obligate, if the insect requires the symbiotic symbiotic interactions, ranging from parasitism to mutualism. relationship for survival, and secondary, or facultative, if the Bacterial symbionts can be found on the surface of the insects relationship is not essential for its survival. However, in some but also inside their bodies (e.g. the gut system). Often, cases, a secondary endosymbiont can act as a coprimary one, mutualistic symbionts and insects establish a more intimate if its presence is also essential for the insect or the primary relationship, where the symbionts are maintained inside spe- endosymbiont (Sudakaran et al. 2017). Although different cialized host cells, called bacteriocytes, that can form an bacterial lineages are capable of establishing a stable ß The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] Genome Biol. Evol. 9(10):2893–2910. doi:10.1093/gbe/evx202 Advance Access publication September 25, 2017 2893 Downloaded from https://academic.oup.com/gbe/article-abstract/9/10/2893/4237403 by Bloomfield Lib for Humanities & Social Sciences. Hebrew University of Jerusalem user on 10 December 2017 Santos-Garcia et al. GBE endosymbiotic relationship with insects, representatives of the 2014; Matsuura et al. 2014; Hosokawa et al. 2015). It is gen- Bacteroidetes as well as Alpha-, Beta-, and erally argued that Sodalis endosymbionts do not play an es- Gammaproteobacteria, especially Enterobacteriaceae,are sential role in the biology of most of their heteropteran hosts, the most prominent groups (Moya et al. 2008; Moran et al. although such functions could not be completely excluded in 2008; Sabree et al. 2009; Husnık et al. 2011; Sudakaran et al. urostylidid stinkbugs, due to the high infection rates in these 2017). species (Kaiwa et al. 2014; Hosokawa et al. 2015). Until pre- Among others, species of the Sodalis group sent, no Sodalis symbiont has been found in the superfamily (Gammaproteobacteria: Enterobacterales: Pectobacteriaceae) Lygaeoidea (reviewed in Sudakaran et al. 2017). The reason offer a spectrum of various types of endosymbiosis. The epon- for this is not clear, because most lygaeoid bugs also harbor a ymous strain was originally described as a secondary endo- broad range of endosymbiotic bacteria accommodated in symbiont of the tsetse fly Glossina morsitans (Dale and specific structures, ranging from midgut crypts to bacter- Maudlin 1999). Because then, numerous different Sodalis or iomes, depending on the (sub)families (Kuechler et al. 2010, Sodalis-allied species were found in several insect groups, 2011, 2012; Kikuchi et al. 2011; Matsuura et al. 2012). such as weevils (Heddi et al. 1999; Oakeson et al. 2014), One of these bacteriome-associated endosymbiosis was hippoboscid louse fly (Novakov aandHyp sa 2007; also described in Henestaris halophilus, a member of the Chrudimsky et al. 2012), chewing lice (Fukatsu et al. 2007; lygaeoid subfamily Henestarinae (Heteroptera: Lygaeoidea: Smith et al. 2013)andseallice(Boyd et al. 2016). In addition, Geocoridae), but has not been analyzed in detail so far hemipteran insects such as aphids (Burke et al. 2009), psyllids (Kuechler et al. 2012). The subfamily Henestarinae is mainly (Sloan and Moran 2012; Arp et al. 2014), scale insects distributed in southern Palearctic and African regions and (Gruwell et al. 2010; Husnık and McCutcheon 2016), spittle- contains about 19 species placed in 3 genera (Schuh and bugs (Koga and Moran 2014), and stinkbugs (Kaiwa et al. Slater 1995). All species, mainly characterized by their stalked 2010, 2011; Matsuura et al. 2014; Hosokawa et al. 2015) eyes, live in saline-affected habitats both inshore and inland. frequently harbor Sodalis endosymbionts. Recently, a The genus Henestaris is phytophagous and H. halophilus Sodalis-allied bacterial strain was also isolated from a human mainly feeds on seeds and infructescence of halophytes, like wound infection (Clayton et al. 2012), possibly representing a Plantago maritima, Artemisia maritima, Aster trifolium or free-living ancestral state of Sodalis. This Sodalis, named Atriplex spp., (Wachmann et al. 2007), but occasionally also Sodalis praecaptivus, and the one from G. morsitans are the on grasses, especially Puccinella distans (Hiebsch 1961). only species cultivable so far. In the present work, we provide the first detailed descrip- Based on their pattern of occurrence in different ecological tion of the bacteriome-associated endosymbiont of H. halo- niches and insects, the “characteristics” of each Sodalis spe- philus, identified as a member of the Sodalis group, including cies and their specific effects on their hosts are quite diverse. molecular characterization, ultrastructural morphology and For example, Sodalis species are often described as facultative localization and transmission route. We also present the endosymbionts, but have also
Load more

Recommended publications
  • An Endosymbiont's Journey Through Metamorphosis of Its Insect Host
    COMMENTARY An endosymbiont’s journey through metamorphosis of its insect host COMMENTARY Martin Kaltenpotha,b,1 Symbiotic microorganisms are essential for the lives of many multicellular eukaryotes (1). In insects, decades of symbiosis and—more recently—microbiome re- search have shown that microbial symbionts can supple- ment limiting nutrients, aid in digestion or detoxification, and defend their host against antagonists, thereby expanding the ecological and evolutionary potential of their hosts (2). In order to ensure that their offspring are endowed with the beneficial symbionts, insects have evolved a range of transmissionroutestopassthesym- bionts vertically from parents to offspring or acquire them horizontally from unrelated host individuals or from the environment (3, 4). However, while, at first glance, the transmission from one host individual to another might seem like the most intricate problem for a symbi- otic partnership, maintaining the symbiosis throughout the host’s development may be no less of a challenge (5). In particular, holometabolous insects like beetles, butterflies and moths, flies, ants, bees, and wasps experience a complete restructuring of the body during metamorphosis from the larva to the adult individual. While gut microbes can be maintained throughout the reorganization of the gut (6), and other extracellular symbionts can persist outside of the host’s body (7), how intracellular mutualists located Fig. 1. (Top) An adult rice weevil (S. oryzae). (Bottom) Schematic representation ’ ’ in special organs (bacteriomes) are maintained and of the symbionts journey during the weevil s metamorphosis and some of the associated gene expression changes in host and symbiont. The gut-associated sometimes even translocated during metamorphosis bacteriome dissociates into individual bacteriocytes (red) in the early pupa, remained poorly understood (but see ref.
    [Show full text]
  • (Pentatomidae) DISSERTATION Presented
    Genome Evolution During Development of Symbiosis in Extracellular Mutualists of Stink Bugs (Pentatomidae) DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Alejandro Otero-Bravo Graduate Program in Evolution, Ecology and Organismal Biology The Ohio State University 2020 Dissertation Committee: Zakee L. Sabree, Advisor Rachelle Adams Norman Johnson Laura Kubatko Copyrighted by Alejandro Otero-Bravo 2020 Abstract Nutritional symbioses between bacteria and insects are prevalent, diverse, and have allowed insects to expand their feeding strategies and niches. It has been well characterized that long-term insect-bacterial mutualisms cause genome reduction resulting in extremely small genomes, some even approaching sizes more similar to organelles than bacteria. While several symbioses have been described, each provides a limited view of a single or few stages of the process of reduction and the minority of these are of extracellular symbionts. This dissertation aims to address the knowledge gap in the genome evolution of extracellular insect symbionts using the stink bug – Pantoea system. Specifically, how do these symbionts genomes evolve and differ from their free- living or intracellular counterparts? In the introduction, we review the literature on extracellular symbionts of stink bugs and explore the characteristics of this system that make it valuable for the study of symbiosis. We find that stink bug symbiont genomes are very valuable for the study of genome evolution due not only to their biphasic lifestyle, but also to the degree of coevolution with their hosts. i In Chapter 1 we investigate one of the traits associated with genome reduction, high mutation rates, for Candidatus ‘Pantoea carbekii’ the symbiont of the economically important pest insect Halyomorpha halys, the brown marmorated stink bug, and evaluate its potential for elucidating host distribution, an analysis which has been successfully used with other intracellular symbionts.
    [Show full text]
  • Effects on Brood Development in the Carpenter Ant Camponotus Vicinus Mayr After Exposure to the Yeast Associate Schwanniomyces Polymorphus Kloecker
    insects Article Effects on Brood Development in the Carpenter Ant Camponotus vicinus Mayr after Exposure to the Yeast Associate Schwanniomyces polymorphus Kloecker Mark E. Mankowski 1,*, Jeffrey J. Morrell 2 and Patricia K. Lebow 3 1 Forest Products Laboratory Starkville, USDA Forest Service, Starkville, MS 39759, USA 2 Centre Timber Durability and Design Life, University of the Sunshine Coast, Sippy Downs, QLD 4102, Australia; [email protected] 3 Forest Products Laboratory Madison, USDA Forest Service, Madison, WI 53726, USA; [email protected] * Correspondence: [email protected] Simple Summary: Carpenter ants are important to ecosystem services as they assist in the breakdown of course woody debris when excavating wood for nests. Feeding on a variety of carbohydrate and protein sources, they have an infrabuccal filter that limits passage of large food particles to their gut. A variety of yeasts have been found associated with the infrabuccal pocket and the nests of these ants. The yeast Schwanniomyces polymorphus is associated with the carpenter ant Camponotus vicinus. To examine a possible nutritional association between this yeast and ant, we reared small sub-colonies of defaunated and non-defaunated C. vincus brood on several artificial diets where various nutritional components were removed. Part of the testing involved exposure of brood to these diets and cells of S. polymorphus. Dietary treatments that were augmented with yeast generally had deleterious Citation: Mankowski, M.E.; Morrell, J.J.; effects on brood development compared to diets without yeast. However, increased brood weight Lebow, P.K. Effects on Brood and increased number of adult ants from initial brood was observed in non-defaunated ants fed a Development in the Carpenter Ant diet where B vitamins and sterols were absent, but augmented with live yeast.
    [Show full text]
  • Serial Horizontal Transfer of Vitamin-Biosynthetic Genes Enables the Establishment of New Nutritional Symbionts in Aphids’ Di-Symbiotic Systems
    The ISME Journal (2020) 14:259–273 https://doi.org/10.1038/s41396-019-0533-6 ARTICLE Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems 1 1 1 2 2 Alejandro Manzano-Marıń ● Armelle Coeur d’acier ● Anne-Laure Clamens ● Céline Orvain ● Corinne Cruaud ● 2 1 Valérie Barbe ● Emmanuelle Jousselin Received: 25 February 2019 / Revised: 24 August 2019 / Accepted: 7 September 2019 / Published online: 17 October 2019 © The Author(s) 2019. This article is published with open access Abstract Many insects depend on obligate mutualistic bacteria to provide essential nutrients lacking from their diet. Most aphids, whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera aphidicola to supply essential amino acids and B vitamins. However, in some aphid species, provision of these nutrients is partitioned between Buchnera and a younger bacterial partner, whose identity varies across aphid lineages. Little is known about the origin and the evolutionary stability of these di-symbiotic systems. It is also unclear whether the novel symbionts merely compensate for losses in Buchnera or 1234567890();,: 1234567890();,: carry new nutritional functions. Using whole-genome endosymbiont sequences of nine Cinara aphids that harbour an Erwinia-related symbiont to complement Buchnera, we show that the Erwinia association arose from a single event of symbiont lifestyle shift, from a free-living to an obligate intracellular one. This event resulted in drastic genome reduction, long-term genome stasis, and co-divergence with aphids. Fluorescence in situ hybridisation reveals that Erwinia inhabits its own bacteriocytes near Buchnera’s. Altogether these results depict a scenario for the establishment of Erwinia as an obligate symbiont that mirrors Buchnera’s.
    [Show full text]
  • 2007151117.Full.Pdf
    Spatial and morphological reorganization of endosymbiosis during metamorphosis accommodates adult metabolic requirements in a weevil Justin Mairea,1, Nicolas Parisota, Mariana Galvao Ferrarinia, Agnès Valliera, Benjamin Gilletb, Sandrine Hughesb, Séverine Balmanda, Carole Vincent-Monégata, Anna Zaidman-Rémya,2, and Abdelaziz Heddia,2 aUMR0203, Biologie Fonctionnelle, Insectes et Interactions (BF2i), Institut National des Sciences Appliquées de Lyon (INSA-Lyon), Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Université de Lyon (Univ Lyon), F-69621 Villeurbanne, France; and bUMR5242, Institut de Génomique Fonctionnelle de Lyon (IGFL), Ecole Normale Supérieure de Lyon, Centre National de la Recherche Scientifique (CNRS), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon (Univ Lyon), F-69007 Lyon, France Edited by John R. Pringle, Stanford University Medical Center, Stanford, CA, and approved June 25, 2020 (received for review April 15, 2020) Bacterial intracellular symbiosis (endosymbiosis) is widespread in allows adaptive decoupling: for example, task specialization of nature and impacts many biological processes. In holometabolous growth at the larval stage versus reproduction at the adult stage symbiotic insects, metamorphosis entails a complete and abrupt (9, 10). However, metamorphosis is also associated with con- internal reorganization that creates a constraint for endosymbiont straints, including higher susceptibility to predators and patho- transmission from larvae to adults. To assess how endosymbiosis gens, as well as the conservation and adaptation of beneficial copes—and potentially evolves—throughout this major host-tissue symbionts (9, 11). In hemimetabolous insects, the relative mor- reorganization, we used the association between the cereal weevil phological stability associated with incomplete metamorphosis is Sitophilus oryzae and the bacterium Sodalis pierantonius as a model believed to facilitate symbiont maintenance and transmission system.
    [Show full text]
  • Easychair Preprint Ant Microbial Endosymbionts and the Emergent
    EasyChair Preprint № 1661 Ant microbial endosymbionts and the emergent properties of social groups Alessio Sclocco, Shirlyn Jia Yun Ong and Serafino Teseo EasyChair preprints are intended for rapid dissemination of research results and are integrated with the rest of EasyChair. October 14, 2019 Ant microbial endosymbionts and the emergent properties of social groups Alessio Sclocco1, Shirlyn Jia Yun Ong2 and Serafino Teseo2† 1Netherlands eScience Center, Amsterdam, The Netherlands (E-mail: [email protected]) 2School of Biological Sciences, Nanyang Technological University, Singapore (Tel: +65 63167088; E-mail: [email protected]) Abstract: In the last fifteen years, research on animal models has provided advances on how gut symbiotic microbes affect behavior and its underlying neurophysiology. However, most studies on the gut microbiota only take into exam individual behavior without considering social dynamics. Contrarily, animals and humans live in complex societies where they constantly adjust physiology and behavior to social interactions. To improve our understanding of how microbes and hosts interact and produce functional individual, social and collective phenotypes, we need to broaden our experimental approaches to a group-level dimension. The ideal models for this purpose are social animals living in stable symbioses with microbes, such as eusocial insects. In our research, we investigate Camponotus carpenter ants and their obligate bacterial symbiont Blochmannia from a behavioral ecology perspective. We aim to create ant colonies including differential proportions of bacteria-free individuals by suppressing Blochmannia with antibiotics. Then, using a machine learning-based video tracking system, we will study network features and group-level behavior of such experimental colonies. Keywords: Social Evolution; Microbiota-Gut-Brain Axis; Ants; Group-Level Behavior; Machine Learning; Real Time Data Analysis 1.
    [Show full text]
  • Table S4. Phylogenetic Distribution of Bacterial and Archaea Genomes in Groups A, B, C, D, and X
    Table S4. Phylogenetic distribution of bacterial and archaea genomes in groups A, B, C, D, and X. Group A a: Total number of genomes in the taxon b: Number of group A genomes in the taxon c: Percentage of group A genomes in the taxon a b c cellular organisms 5007 2974 59.4 |__ Bacteria 4769 2935 61.5 | |__ Proteobacteria 1854 1570 84.7 | | |__ Gammaproteobacteria 711 631 88.7 | | | |__ Enterobacterales 112 97 86.6 | | | | |__ Enterobacteriaceae 41 32 78.0 | | | | | |__ unclassified Enterobacteriaceae 13 7 53.8 | | | | |__ Erwiniaceae 30 28 93.3 | | | | | |__ Erwinia 10 10 100.0 | | | | | |__ Buchnera 8 8 100.0 | | | | | | |__ Buchnera aphidicola 8 8 100.0 | | | | | |__ Pantoea 8 8 100.0 | | | | |__ Yersiniaceae 14 14 100.0 | | | | | |__ Serratia 8 8 100.0 | | | | |__ Morganellaceae 13 10 76.9 | | | | |__ Pectobacteriaceae 8 8 100.0 | | | |__ Alteromonadales 94 94 100.0 | | | | |__ Alteromonadaceae 34 34 100.0 | | | | | |__ Marinobacter 12 12 100.0 | | | | |__ Shewanellaceae 17 17 100.0 | | | | | |__ Shewanella 17 17 100.0 | | | | |__ Pseudoalteromonadaceae 16 16 100.0 | | | | | |__ Pseudoalteromonas 15 15 100.0 | | | | |__ Idiomarinaceae 9 9 100.0 | | | | | |__ Idiomarina 9 9 100.0 | | | | |__ Colwelliaceae 6 6 100.0 | | | |__ Pseudomonadales 81 81 100.0 | | | | |__ Moraxellaceae 41 41 100.0 | | | | | |__ Acinetobacter 25 25 100.0 | | | | | |__ Psychrobacter 8 8 100.0 | | | | | |__ Moraxella 6 6 100.0 | | | | |__ Pseudomonadaceae 40 40 100.0 | | | | | |__ Pseudomonas 38 38 100.0 | | | |__ Oceanospirillales 73 72 98.6 | | | | |__ Oceanospirillaceae
    [Show full text]
  • Diversity of Pectobacteriaceae Species in Potato Growing Regions in Northern Morocco
    microorganisms Article Diversity of Pectobacteriaceae Species in Potato Growing Regions in Northern Morocco Saïd Oulghazi 1,2, Mohieddine Moumni 1, Slimane Khayi 3 ,Kévin Robic 2,4, Sohaib Sarfraz 5, Céline Lopez-Roques 6,Céline Vandecasteele 6 and Denis Faure 2,* 1 Department of Biology, Faculty of Sciences, Moulay Ismaïl University, 50000 Meknes, Morocco; [email protected] (S.O.); [email protected] (M.M.) 2 Institute for Integrative Biology of the Cell (I2BC), Université Paris-Saclay, CEA, CNRS, 91198 Gif-sur-Yvette, France; [email protected] 3 Biotechnology Research Unit, CRRA-Rabat, National Institut for Agricultural Research (INRA), 10101 Rabat, Morocco; [email protected] 4 National Federation of Seed Potato Growers (FN3PT-RD3PT), 75008 Paris, France 5 Department of Plant Pathology, University of Agriculture Faisalabad Sub-Campus Depalpur, 38000 Okara, Pakistan; [email protected] 6 INRA, US 1426, GeT-PlaGe, Genotoul, 31320 Castanet-Tolosan, France; [email protected] (C.L.-R.); [email protected] (C.V.) * Correspondence: [email protected] Received: 28 April 2020; Accepted: 9 June 2020; Published: 13 June 2020 Abstract: Dickeya and Pectobacterium pathogens are causative agents of several diseases that affect many crops worldwide. This work investigated the species diversity of these pathogens in Morocco, where Dickeya pathogens have only been isolated from potato fields recently. To this end, samplings were conducted in three major potato growing areas over a three-year period (2015–2017). Pathogens were characterized by sequence determination of both the gapA gene marker and genomes using Illumina and Oxford Nanopore technologies.
    [Show full text]
  • Hemiptera: Adelgidae)
    The ISME Journal (2012) 6, 384–396 & 2012 International Society for Microbial Ecology All rights reserved 1751-7362/12 www.nature.com/ismej ORIGINAL ARTICLE Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/piceae complex (Hemiptera: Adelgidae) Elena R Toenshoff1, Thomas Penz1, Thomas Narzt2, Astrid Collingro1, Stephan Schmitz-Esser1,3, Stefan Pfeiffer1, Waltraud Klepal2, Michael Wagner1, Thomas Weinmaier4, Thomas Rattei4 and Matthias Horn1 1Department of Microbial Ecology, University of Vienna, Vienna, Austria; 2Core Facility, Cell Imaging and Ultrastructure Research, University of Vienna, Vienna, Austria; 3Department of Veterinary Public Health and Food Science, Institute for Milk Hygiene, Milk Technology and Food Science, University of Veterinary Medicine Vienna, Vienna, Austria and 4Department of Computational Systems Biology, University of Vienna, Vienna, Austria Adelgids (Insecta: Hemiptera: Adelgidae) are known as severe pests of various conifers in North America, Canada, Europe and Asia. Here, we present the first molecular identification of bacteriocyte-associated symbionts in these plant sap-sucking insects. Three geographically distant populations of members of the Adelges nordmannianae/piceae complex, identified based on coI and ef1alpha gene sequences, were investigated. Electron and light microscopy revealed two morphologically different endosymbionts, coccoid or polymorphic, which are located in distinct bacteriocytes. Phylogenetic analyses of their 16S and 23S rRNA gene sequences assigned both symbionts to novel lineages within the Gammaproteobacteria sharing o92% 16S rRNA sequence similarity with each other and showing no close relationship with known symbionts of insects. Their identity and intracellular location were confirmed by fluorescence in situ hybridization, and the names ‘Candidatus Steffania adelgidicola’ and ‘Candidatus Ecksteinia adelgidicola’ are proposed for tentative classification.
    [Show full text]
  • The Role of the Microbiome in Oral Squamous Cell Carcinoma with Insight Into the Microbiome–Treatment Axis
    International Journal of Molecular Sciences Review The Role of the Microbiome in Oral Squamous Cell Carcinoma with Insight into the Microbiome–Treatment Axis Amel Sami 1,2, Imad Elimairi 2,* , Catherine Stanton 1,3, R. Paul Ross 1 and C. Anthony Ryan 4 1 APC Microbiome Ireland, School of Microbiology, University College Cork, Cork T12 YN60, Ireland; [email protected] (A.S.); [email protected] (C.S.); [email protected] (R.P.R.) 2 Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, National Ribat University, Nile Street, Khartoum 1111, Sudan 3 Teagasc Food Research Centre, Moorepark, Fermoy, Cork P61 C996, Ireland 4 Department of Paediatrics and Child Health, University College Cork, Cork T12 DFK4, Ireland; [email protected] * Correspondence: [email protected] Received: 30 August 2020; Accepted: 12 October 2020; Published: 29 October 2020 Abstract: Oral squamous cell carcinoma (OSCC) is one of the leading presentations of head and neck cancer (HNC). The first part of this review will describe the highlights of the oral microbiome in health and normal development while demonstrating how both the oral and gut microbiome can map OSCC development, progression, treatment and the potential side effects associated with its management. We then scope the dynamics of the various microorganisms of the oral cavity, including bacteria, mycoplasma, fungi, archaea and viruses, and describe the characteristic roles they may play in OSCC development. We also highlight how the human immunodeficiency viruses (HIV) may impinge on the host microbiome and increase the burden of oral premalignant lesions and OSCC in patients with HIV. Finally, we summarise current insights into the microbiome–treatment axis pertaining to OSCC, and show how the microbiome is affected by radiotherapy, chemotherapy, immunotherapy and also how these therapies are affected by the state of the microbiome, potentially determining the success or failure of some of these treatments.
    [Show full text]
  • DNA Transduction in Sodalis Species: Implications for the Genetic
    bioRxiv preprint doi: https://doi.org/10.1101/2020.12.02.408930; this version posted December 7, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 DNA transduction in Sodalis species: implications for the genetic 2 modification of uncultured endosymbionts of insects 3 4 5 Chelsea M. Keller1, Christopher G. Kendra1, Roberto E. Bruna1, David Craft1, Mauricio 6 H. Pontes1,2* 7 8 9 1Department of Pathology and Laboratory Medicine, 2Department of Microbiology and 10 Immunology, Pennsylvania State University College of Medicine, Hershey, PA 17033, 11 USA. 12 13 *Corresponding author: 14 Mauricio H. Pontes 15 Penn State College of Medicine 16 Departments of Pathology, and 17 Microbiology and Immunology 18 500 University Drive, C6818A 19 Hershey, PA 17033 20 [email protected] 21 717-531-0003 ext. 320524 22 23 Running title: Bacteriophage P1-mediated transduction in Sodalis 24 bioRxiv preprint doi: https://doi.org/10.1101/2020.12.02.408930; this version posted December 7, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 25 Abstract 26 Bacteriophages (phages) are ubiquitous in nature. These viruses play a number of 27 central roles in microbial ecology and evolution by, for instance, promoting horizontal 28 gene transfer (HGT) among bacterial species.
    [Show full text]
  • Serratia Symbiotica and Aphids 1 2 Julie Perreaua,B, Devki J. Patela
    bioRxiv preprint doi: https://doi.org/10.1101/2020.09.01.279018; this version posted September 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Vertical transmission at the pathogen-symbiont interface: Serratia symbiotica and aphids 2 3 Julie Perreaua,b, Devki J. Patela, Hanna Andersona, Gerald P. Maedaa, Katherine M. Elstonb, 4 Jeffrey E. Barrickb, Nancy A. Morana 5 6 a Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712 7 b Department of Molecular Biosciences, University of Texas at Austin, Austin, TX 78712 8 9 Running title: Serratia symbiotica at the pathogen-symbiont interface 10 11 # Address correspondence to Julie Perreau, [email protected] 12 13 14 Word count 15 Abstract: 236 16 Text (excluding the references, table footnotes, and figure legends): 5,098 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.09.01.279018; this version posted September 2, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 17 Abstract 18 Many insects possess beneficial bacterial symbionts that occupy specialiZed host cells and are 19 maternally transmitted. As a consequence of their host-restricted lifestyle, these symbionts often 20 possess reduced genomes and cannot be cultured outside hosts, limiting their study.
    [Show full text]