Spaceflight Imposes Numerous Adaptive Challenges for Terrestrial Life

Total Page:16

File Type:pdf, Size:1020Kb

Spaceflight Imposes Numerous Adaptive Challenges for Terrestrial Life Astrobiology Science Conference 2017 (LPI Contrib. No. 1965) 3032.pdf Transcriptomic changes in an animal-bacterial symbiosis under modeled microgravity conditions. Giorgio Casaburi1, Irina Goncharenko-Foster1 and Jamie S. Foster1, 1Department of Microbiology and Cell Science, University of Florida, Space Life Science Lab, Merritt Island, FL, USA. Introduction: Spaceflight imposes numerous adaptive challenges for terrestrial life. The reduction in gravity, or microgravity, represents a novel environ- ment that can disrupt homeostasis of many physiologi- cal processes. Additionally, it is becoming increasingly clear that an organism’s microbiome is critical for host health and examining its resiliency in microgravity represents a new frontier for space biology research. In this study, we examine the impact of microgravity on the interactions between the squid Euprymna scolopes and its beneficial symbiont Vibrio fischeri, which form a highly specific binary mutualism. First, animals in- oculated with V. fischeri aboard the space shuttle showed effective colonization of the host light organ, the site of the symbiosis, during space flight. Second, RNA-Seq analysis of squid exposed to modeled mi- crogravity conditions exhibited extensive differential gene expression in the presence and absence of the symbiotic partner. Transcriptomic analyses revealed in the absence of the symbiont during modeled micro- gravity there was an enrichment of genes and pathways associated with the innate immune and oxidative stress response. The results suggest that V. fischeri may help modulate the host stress responses under modeled mi- crogravity. This study provides a window into the adaptive responses that the host animal and its symbi- ont use during modeled microgravity. .
Recommended publications
  • Octopus Insularis</Italic> As a New Marine Model for Evolutionary
    © 2019. Published by The Company of Biologists Ltd | Biology Open (2019) 8, bio046086. doi:10.1242/bio.046086 RESEARCH ARTICLE Octopus insularis as a new marine model for evolutionary developmental biology Ernesto Maldonado1,*, Emma Rangel-Huerta1,2, Roberto González-Gómez3,4, Gabriel Fajardo-Alvarado3,4 and Piedad S. Morillo-Velarde4,5,* ABSTRACT of aquatic animal eggs and embryos guarantees the observation of Octopuses are intriguing organisms that, together with squids and every developmental stage using microscopy and allows detailed cuttlefishes, form the extant coleoid cephalopods. This group includes experimental analysis from the first cell division through to the many species that can potentially be used as models in the fields of formation of embryonic germ layers and organogenesis (Boletzky biomedicine, developmental biology, evolution, neuroscience and et al., 2006). Finally, small embryos allow reasonable sample sizes even for robotics research. The purpose of this work is to first to be tested together using multi-well plates to provide multiple present a simple method for maintaining Octopus insularis embryos experimental replicates at the same time, making them cost- under a laboratory setup. Second, we show that these embryos are effective animal models (Hill et al., 2005). suitable for detailed analyses of specific traits that appear during Coleoid cephalopods (octopus, squid and cuttlefish) exhibit the developmental stages, including the eyes, hearts, arms, suckers, largest nervous systems found among invertebrates (Young, 1971) chromatophores and Kölliker’s organs. Similar complex traits between and a sophisticated visual system controlling body color changes for cephalopods and vertebrates such as the visual, cardiovascular, communication, camouflage and mimicry (Hanlon et al., 2011; neural and pigmentation systems are generally considered to be a Robin et al., 2014).
    [Show full text]
  • Counterillumination in the Hawaiian Bobtail Squid, Euprymna Scolopes Berry (Mollusca: Cephalopoda)
    Marine Biology (2004) 144: 1151–1155 DOI 10.1007/s00227-003-1285-3 RESEARCH ARTICLE B. W. Jones Æ M. K. Nishiguchi Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda) Received: 27 May 2003 / Accepted: 24 November 2003 / Published online: 10 January 2004 Ó Springer-Verlag 2004 Abstract The mutualism between the Hawaiian bobtail 1999), predator evasion (Hartline et al. 1999), and squid Euprymna scolopes and the luminescent symbiont counterillumination, an antipredatory behavior com- Vibrio fischeri has been used extensively as a model mon to many midwater cephalopods, decapod crusta- system for studies ranging from co-speciation and bio- ceans, and fishes (Young 1977; Harper and Case 1999; geography to gene regulation and the evolution of Lindsay et al. 1999). Animals exhibiting counterillumi- pathogenesis. In this association, the luminescent bac- nation reduce their silhouette by producing biolumi- terium V. fischeri is housed in a complex light organ nescence in an attempt to match the intensity and within the mantle cavity of E. scolopes. Prior hypotheses wavelength of down-welling light (Young and Roper have assumed that sepiolid squids in general utilize the 1977), providing a mechanism that allows them to evade bioluminescence produced by their V. fischeri symbionts predators by camouflage. The light produced can either for counterillumination, a behavior that helps squid be autogenic (luminescence produced intrinsically by the camouflage themselves by matching down-welling animal itself), or bacteriogenic (produced by bacterial moonlight via silhouette reduction. This assumption, symbionts). based solely on the morphology of the squid light organ, Establishing a morphological design for efficient has never been empirically tested for Euprymna in the counterillumination has resulted in the evolution of a laboratory.
    [Show full text]
  • Glossary for Hawaiian and Other Polynesian Terms
    Glossary for Hawaiian and Other Polynesian Terms Pronunciation Hawaiian vowels are as in English: a, e, i, o, and u. But with respect to pronunciation, the letter “a” is pronounced as the soft ah sound in papa; “e” as the ā sound in play; “i” as the ē sound in need; “o” as used in bowl; and “u” as the ew sound in tune. Diacritical marks are used to indicate stress on particular vowels, and as glottal stops. Te macron (called kahakō in Hawaiian) is used to stress and elongate any of the vowel sounds. For example, the ā sound in pāhoe- hoe (sheet lava) is stressed and lengthened, as in pahh-ho-ay-ho-ay. Te reverse apostrophe (called an okina in Hawaiian) is used as a glot- tal stop, as in the closed throat sound that should precede formation of the word ‘ahi (pronounced ah-hee), or between sounds, as in Punalu‘u (pronounced poo-nah-lew-ew). Certain vowel combinations (diph- thongs) are also pronounced in a manner dissimilar to the way they are pronounced in English, with stress on the frst vowel. For instance, the “ou” sound in Hawaiian is pronounced with stress on the o, as in pouli © Te Editor(s) (if applicable) and Te Author(s), under exclusive license 247 to Springer Nature Switzerland AG 2019 E. W. Glazier, Tradition-Based Natural Resource Management, Palgrave Studies in Natural Resource Management, https://doi.org/10.1007/978-3-030-14842-3 248 Glossary for Hawaiian and Other Polynesian Terms (Hawaiian for dark or eclipse, pronounced poh-lee).
    [Show full text]
  • Cover Image the Hawaiian Bobtail Squid
    SUBSCRIPTIONS In 2020 Phil. Trans. R. Soc. B (ISSN 0962-8436) will be published Continuing its long history of infl uential scientifi c publishing, Phil. Trans. R. Soc. B 26 times a year. For more details of publishes high quality theme issues on topics of current importance and general subscriptions and single issue sales interest within the life sciences, guest-edited by leading authorities and comprising please contact our fulfi lment agent: new research, reviews and opinions from prominent researchers. Each issue Turpin Distribution aims to create an original and authoritative synthesis, often bridging traditional The Royal Society Customer Services Pegasus Drive disciplines, which showcases current developments and provides a foundation for Stratton Business Park future research, applications and policy decisions. Biggleswade SG18 8TQ United Kingdom royalsocietypublishing.org/journal/rstb T +44 1767 604951 F +44 1767 601640 E [email protected] EDITOR Karen Lipkow Alternatively, please contact our customer John Pickett Karen Liu service team at: Satyajit Mayor E [email protected] SENIOR COMMISSIONING EDITOR Ewa Paluch Helen Eaton Ricard Solé PRICES FOR 2020 Roland Wedlich-Söldner PRODUCTION EDITOR Online Online Garrett Ziolek Neuroscience and cognition only and print Dora Biro EDITORIAL BOARD Anna Borghi £ UK/rest of World £2812 £3936 Organismal, environmental Nicole Creanza and evolutionary biology Patricia Pestana Garcez € Europe €3656 €5118 Julia Blanchard Anthony Isles $ US/Canada $5323 $7452 Patrick Butler
    [Show full text]
  • Identification and Gene Expression of Multiple Peptidoglycan Recognition
    Identification and gene expression of multiple peptidoglycan recognition proteins (PGRPs) in the deep-sea mussel Bathymodiolus azoricus, involvement in symbiosis? Camille Détrée, François H. Lallier, Arnaud Tanguy, Jean Mary To cite this version: Camille Détrée, François H. Lallier, Arnaud Tanguy, Jean Mary. Identification and gene expression of multiple peptidoglycan recognition proteins (PGRPs) in the deep-sea mussel Bathymodiolus azoricus, involvement in symbiosis?. Comparative Biochemistry and Physiology - Part B: Biochemistry and Molecular Biology, Elsevier, 2017, 207, pp.1-8. 10.1016/j.cbpb.2017.02.002. hal-01469197 HAL Id: hal-01469197 https://hal.sorbonne-universite.fr/hal-01469197 Submitted on 16 Feb 2017 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. ACCEPTED MANUSCRIPT Détrée et al. 2017 Identification and gene expression of multiple peptidoglycan recognition proteins (PGRPs) in the deep-sea mussel Bathymodiolus azoricus, involvement in symbiosis? Camille Détrée1,2, François H. Lallier1, Arnaud Tanguy1, Jean Mary1,* 1Sorbonne Universités, UPMC Univ Paris 06, CNRS UMR 7144, Adaptation et Diversité en Milieu Marin, Equipe ABICE, Station Biologique de Roscoff, 29680 Roscoff, France 2Present address: Laboratory of Biotechnology and Aquatic Genomics, Interdisciplinary Center for Aquaculture Research (INCAR), University of Concepcion, Concepción, Chile Running title: Bathymodiolus azoricus’s PGRPs and regulation of the symbiosis * Corresponding author: Dr.
    [Show full text]
  • Immune Protein Orchestrates Daily Rhythm of Squid-Bacteria Symbiotic Relationship 19 October 2020, by Marcie Grabowski
    Immune protein orchestrates daily rhythm of squid-bacteria symbiotic relationship 19 October 2020, by Marcie Grabowski National Academy of Sciences, could provide important clues on factors affecting human microbiome rhythms, as the MIF protein is also found in abundance in mammalian symbiotic tissues. To survive, the nocturnal Hawaiian bobtail squid depends on V. fischeri, which gives it the ability to mimic moonlight on the surface of the ocean and deceive monk seals and other predators, as it forages for food. The symbiotic bacteria also require nutrition, especially at night when they are more numerous and their light is required for the squid's camouflage. The research team, led by Eric Koch, who was a graduate researcher at the Pacific Biosciences Research Center (PBRC) in the UH Manoa School of Ocean and Earth Science and Technology (SOEST) at the time of the study, determined the squid regulates production of MIF as a way to A 63x magnification image showing the 4-week-old light control the movement of specialized immune cells, organ during the day showing EsMIF (magenta) called hemocytes, which provide chitin for bacteria surrounding the crypt spaces. Host DNA is labeled in to feed on. blue and the bacteria are labeled in green. Credit: Eric Koch At night, when the team found MIF was low in the squid's light organ, hemocytes were allowed into the regions where the bacteria reside and chitin was delivered. During the day, MIF was very high, Nearly every organism hosts a collection of which inhibits the hemocytes from coming into the symbiotic microbes—a microbiome.
    [Show full text]
  • Phylogeny and Fitness of Vibrio Fischeri from the Light Organs of Euprymna Scolopes in Two Oahu, Hawaii Populations
    The ISME Journal (2012) 6, 352–362 & 2012 International Society for Microbial Ecology All rights reserved 1751-7362/12 www.nature.com/ismej ORIGINAL ARTICLE Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu, Hawaii populations Michael S Wollenberg and Edward G Ruby Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI, USA The evolutionary relationship among Vibrio fischeri isolates obtained from the light organs of Euprymna scolopes collected around Oahu, Hawaii, were examined in this study. Phylogenetic reconstructions based on a concatenation of fragments of four housekeeping loci (recA, mdh, katA, pyrC) identified one monophyletic group (‘Group-A’) of V. fischeri from Oahu. Group-A V. fischeri strains could also be identified by a single DNA fingerprint type. V. fischeri strains with this fingerprint type had been observed to be at a significantly higher abundance than other strains in the light organs of adult squid collected from Maunalua Bay, Oahu, in 2005. We hypothesized that these previous observations might be related to a growth/survival advantage of the Group-A strains in the Maunalua Bay environments. Competition experiments between Group-A strains and non- Group-A strains demonstrated an advantage of the former in colonizing juvenile Maunalua Bay hosts. Growth and survival assays in Maunalua Bay seawater microcosms revealed a reduced fitness of Group-A strains relative to non-Group-A strains. From these results, we hypothesize that there may exist trade-offs between growth in the light organ and in seawater environments for local V. fischeri strains from Oahu.
    [Show full text]
  • A Genomic Comparison of 13 Symbiotic Vibrio Fischeri Isolates from the Perspective of Their Host Source and Colonization Behavior
    The ISME Journal (2016) 10, 2907–2917 © 2016 International Society for Microbial Ecology All rights reserved 1751-7362/16 www.nature.com/ismej ORIGINAL ARTICLE A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior Clotilde Bongrand1,3, Eric J Koch1,3, Silvia Moriano-Gutierrez1,3, Otto X Cordero2, Margaret McFall-Ngai1,3, Martin F Polz2 and Edward G Ruby1,3 1Department of Medical Microbiology and Immunology, University of Wisconsin-Madison, Madison, WI, USA and 2Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA Newly hatched Euprymna scolopes squid obtain their specific light-organ symbionts from an array of Vibrio (Allivibrio) fischeri strains present in their environment. Two genetically distinct populations of this squid species have been identified, one in Kaneohe Bay (KB), and another in Maunaloa Bay (MB), Oahu. We asked whether symbionts isolated from squid in each of these populations outcompete isolates from the other population in mixed-infection experiments. No relationship was found between a strain’s host source (KB or MB) and its ability to competitively colonize KB or MB juveniles in a mixed inoculum. Instead, two colonization behaviors were identified among the 11 KB and MB strains tested: a ‘dominant’ outcome, in which one strain outcompetes the other for colonization, and a ‘sharing’ outcome, in which two strains co-colonize the squid. A genome-level comparison of these and other V. fischeri strains suggested that the core genomic structure of this species is both syntenous and highly conserved over time and geographical distance.
    [Show full text]
  • Understanding the Cephalopod Immune System Based on Functional and Molecular Evidence
    Understanding the cephalopod immune system based on functional and molecular evidence C. Gestal1* and S. Castellanos-Martínez1,2 1Instituto de Investigaciones Marinas (CSIC). Eduardo Cabello 6, 36208 Vigo, Spain. 2Present address: Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del IPN Unidad Mérida, Antigua carretera a Progreso Km. 6, 97310, Mérida, Yucatán, México *Corresponding Author: Camino Gestal Instituto de Investigaciones Marinas (CSIC) Eduardo Cabello 6 36208 Vigo, Spain. Tf. +34 986 231930 Ext. 290 e-mail: [email protected] ABSTRACT Cephalopods have the most advanced circulatory and nervous system among the mollusks. Recently, they have been included in the European directive which state that suffering and pain should be minimized in cephalopods used in experimentation. The knowledge about cephalopod welfare is still limited and several gaps are yet to be filled, especially in reference to pathogens, pathologies and immune response of these mollusks. In light of the requirements of the normative, in addition to the ecologic and economic importance of cephalopods, in this review we update the work published to date concerning cephalopod immune system. Significant advances have been reached in relation to the characterization of haemocytes and defensive mechanisms comprising cellular and humoral factors mainly, but not limited, in species of high economic value like Sepia officinalis and Octopus vulgaris. Moreover, the improvement of molecular approaches has helped to discover several immune-related genes/proteins. These immune genes/proteins include antimicrobial peptides, phenoloxidases, antioxidant enzymes, serine protease inhibitor, lipopolysaccharide-induced TNF-α factor, Toll-like receptors, lectins, even clusters of differentiation among others. Most of them have been found in haemocytes but also in gills and digestive gland, and the characterization as well as their precise role in the immune response of cephalopods is still pending to be elucidated.
    [Show full text]
  • View: Mammalian Peptidoglycan Recognition Proteins (Pgrps) in Innate Immunity
    Zhang et al. BMC Veterinary Research (2019) 15:10 https://doi.org/10.1186/s12917-018-1744-1 RESEARCH ARTICLE Open Access Molecular characterization and expression analysis of two peptidoglycan recognition proteins (CcPGRP5, CcPGRP6) in larvae ontogeny of common carp Cyprinus carpio L. and upon immune stimulation by bacteria Fumiao Zhang†, Shijuan Shan†, Xiaoyang Xu, Yao Wang, Yonghuan Zhang, Miao Yin* and Guiwen Yang* Abstract Background: Although teleost fish developed acquired immunity firstly in evolution, innate immunity is still very important for them. Innate immunity depends on pattern recognition receptors (PRRs) to distinguish “self” and “non-self”, Peptidoglycan (PGN) recognition protein (PGRP) is one of the receptors and it can bind to multiple components of bacterial envelope. Results: We report the cloning and expression analysis of two PGRPs (Ccpgrp5 and Ccpgrp6) from common carp (Cyprinus carpio L). The Ccpgrp5 gene encodes a protein of 199 amino acid (aa) with PGRP domain, Ami_2 domain and four Zn2+ binding sites required for amidase activity, but without signal peptide and transmembrane domain. The Ccpgrp6 gene encodes a protein of 446 aa with PGRP domain, Ami_2 domain, signal peptide, five Zn2+ binding sites required for amidase activity and two sites for N-glycosylation. The phylogenetic analysis revealed that the CcPGRP5 and CcPGRP6 are closely related to Ctenopharyngodon idella and Danio rerio. Ccpgrp5 and Ccpgrp6 were expressed in all tissues examined including liver, spleen, muscle, oral epithelium, head kidney, gill, skin, gonad, brain, foregut and hindgut and showed different distribution characteristics. During the embryonic and early larval developmental stages of common carp, Ccpgrp6 was detected to be highly expressed at 10 days post fertilization(dpf) and 36 dpf, while Ccpgrp5 were hardly detected using Real-time quantitative PCR.
    [Show full text]
  • The Euprymna Scolopes -Vibrio Fischeri Symbiosis: a Biomedical Model for the Study of Bacterial Colonization of Animal Tissue
    J. Molec. Microbiol. Biotechnol. (1999) 1(1): 13-21. The Squid-Vibrio SymbiosisJMMB as a Biomedical Symposium Model 13 The Euprymna scolopes -Vibrio fischeri Symbiosis: A Biomedical Model for the Study of Bacterial Colonization of Animal Tissue Edward G. Ruby* biological world. The principal interactions between bacteria and animal Pacific Biomedical Research Center tissue occur along the apical surfaces of host epithelial University of Hawaii, Manoa, Hawaii cells. Typically, a diverse consortium of microorganisms and host cells forms a dynamic, cooperating unit that helps maintain a healthy microenvironment within the colonized Abstract tissues. Such associations are ubiquitous, exhibit species specificity and, with few exceptions (Breznak and Brune, The diversity of microorganisms found in the marine 1994; Whittaker et al., 1996; Hooper et al., 1998), are poorly environment reflects the immense size, range of understood. A better understanding of the process by which physical conditions and energy sources, and bacteria and host cells exchange the signals that underlie evolutionary age of the sea. Because associations with these phenomena is an important research goal of living animal tissue are an important and ancient part biomedical research. Over the past decade the E. scolopes- of the ecology of many microorganisms, it is not V. fischeri association, a natural and experimentally facile surprising that the study of marine symbioses model system, has been used to discover the nature of (including both cooperative and pathogenic the mechanisms by which animals form beneficial interactions) has produced numerous discoveries of associations with microorganisms, and to determine how biotechnological and biomedical significance. The these mechanisms are related to, but have diverged from, association between the bioluminescent bacterium those that function in pathogenic infections.
    [Show full text]
  • Cephalopod Guidelines
    Reference Resources Caveats from AAALAC’s Council on Accreditation regarding this resource: Guidelines for the Care and Welfare of Cephalopods in Research– A consensus based on an initiative by CephRes, FELASA and the Boyd Group *This reference was adopted by the Council on Accreditation with the following clarification and exceptions: The AAALAC International Council on Accreditation has adopted the “Guidelines for the Care and Welfare of Cephalopods in Research- A consensus based on an initiative by CephRes, FELASA and the Boyd Group” as a Reference Resource with the following two clarifications and one exception: Clarification: The acceptance of these guidelines as a Reference Resource by AAALAC International pertains only to the technical information provided, and not the regulatory stipulations or legal implications (e.g., European Directive 2010/63/EU) presented in this article. AAALAC International considers the information regarding the humane care of cephalopods, including capture, transport, housing, handling, disease detection/ prevention/treatment, survival surgery, husbandry and euthanasia of these sentient and highly intelligent invertebrate marine animals to be appropriate to apply during site visits. Although there are no current regulations or guidelines requiring oversight of the use of invertebrate species in research, teaching or testing in many countries, adhering to the principles of the 3Rs, justifying their use for research, commitment of appropriate resources and institutional oversight (IACUC or equivalent oversight body) is recommended for research activities involving these species. Clarification: Page 13 (4.2, Monitoring water quality) suggests that seawater parameters should be monitored and recorded at least daily, and that recorded information concerning the parameters that are monitored should be stored for at least 5 years.
    [Show full text]