In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides

被引:105
作者
Fraune, Sebastian [1 ]
Augustin, Rene [1 ]
Anton-Erxleben, Friederike [1 ]
Wittlieb, Joerg [1 ]
Gelhaus, Christoph [1 ]
Klimovich, Vladimir B. [2 ]
Samoilovich, Marina P. [2 ]
Bosch, Thomas C. G. [1 ]
机构
[1] Univ Kiel, Inst Zool, D-24098 Kiel, Germany
[2] Cent Res Inst Roentgeno Radiol, Hybridoma Technol Lab, St Petersburg 189646, Russia
关键词
innate immunity; host-microbe interaction; embryo protection; cnidaria; Hydra; LOLIGO-OPALESCENS; STEM-CELLS; HYDRA; EMBRYOGENESIS; DEFENSE; GENES; EGGS; DIFFERENTIATION; FERTILIZATION; TRANSMISSION;
D O I
10.1073/pnas.1008573107
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Early embryos of many organisms develop outside the mother and are immediately confronted with myriads of potential colonizers. How these naive developmental stages control and shape the bacterial colonization is largely unknown. Here we show that early embryonic stages of the basal metazoan Hydra are able to control bacterial colonization by using maternal antimicrobial peptides. Antimicrobial peptides of the periculin family selecting for a specific bacterial colonization during embryogenesis are produced in the oocyte and in early embryos. If overexpressed in hydra ectodermal epithelial cells, periculin 1a drastically reduces the bacterial load, indicating potent antimicrobial activity. Unexpectedly, transgenic polyps also revealed that periculin, in addition to bactericidal activity, changes the structure of the bacterial community. These findings delineate a role for antimicrobial peptides both in selecting particular bacterial partners during development and as important components of a "be prepared" strategy providing transgenerational protection.
引用
收藏
页码:18067 / 18072
页数:6
相关论文
共 43 条
  • [1] Plasticity of epithelial cell shape in response to upstream signals: A whole-organism study using transgenic Hydra
    Anton-Erxleben, Friederike
    Thomas, Antje
    Wittlieb, Joerg
    Fraune, Sebastian
    Bosch, Thomas C. G.
    [J]. ZOOLOGY, 2009, 112 (03) : 185 - 194
  • [2] PRIMROSE: a computer program for generating and estimating the phylogenetic range of 16S rRNA oligonucleotide probes and primers in conjunction with the RDP-II database
    Ashelford, KE
    Weightman, AJ
    Fry, JC
    [J]. NUCLEIC ACIDS RESEARCH, 2002, 30 (15) : 3481 - 3489
  • [3] Dickkopf related genes are components of the positional value gradient in hydra
    Augustin, Rene
    Franke, Andre
    Khalturin, Konstantin
    Kiko, Rainer
    Siebert, Stefan
    Hemmrich, Georg
    Bosch, Thomas C. G.
    [J]. DEVELOPMENTAL BIOLOGY, 2006, 296 (01) : 62 - 70
  • [4] How Hydra senses and destroys microbes
    Augustin, Rene
    Fraune, Sebastian
    Bosch, Thomas C. G.
    [J]. SEMINARS IN IMMUNOLOGY, 2010, 22 (01) : 54 - 58
  • [5] Activity of the Novel Peptide Arminin against Multiresistant Human Pathogens Shows the Considerable Potential of Phylogenetically Ancient Organisms as Drug Sources
    Augustin, Rene
    Anton-Erxleben, Friederike
    Jungnickel, Stephanie
    Hemmrich, Georg
    Spudy, Bjoern
    Podschun, Rainer
    Bosch, Thomas C. G.
    [J]. ANTIMICROBIAL AGENTS AND CHEMOTHERAPY, 2009, 53 (12) : 5245 - 5250
  • [6] Antifungal skin bacteria, embryonic survival, and communal nesting in four-toed salamanders, Hemidactylium scutatum
    Banning, Jenifer L.
    Weddle, Anna L.
    Wahl, George W., III
    Simon, Mary Alice
    Lauer, Antje
    Walters, Robert L.
    Harris, Reid N.
    [J]. OECOLOGIA, 2008, 156 (02) : 423 - 429
  • [7] Cutaneous Bacteria of the Redback Salamander Prevent Morbidity Associated with a Lethal Disease
    Becker, Matthew H.
    Harris, Reid N.
    [J]. PLOS ONE, 2010, 5 (06):
  • [8] EGG CAPSULE SHEATH OF LOLIGO-OPALESCENS BERRY - STRUCTURE AND ASSOCIATION WITH BACTERIA
    BIGGS, J
    EPEL, D
    [J]. JOURNAL OF EXPERIMENTAL ZOOLOGY, 1991, 259 (02): : 263 - 267
  • [9] Uncovering the evolutionary history of innate immunity: The simple metazoan Hydra uses epithelial cells for host defence
    Bosch, Thomas C. G.
    Augustin, Rene
    Anton-Erxleben, Friederike
    Fraune, Sebastian
    Hemmrich, Georg
    Zill, Holger
    Rosenstiel, Philip
    Jacobs, Gunnar
    Schreiber, Stefan
    Leippe, Matthias
    Stanisak, Mareike
    Groetzinger, Joachim
    Jung, Sascha
    Podschun, Rainer
    Bartels, Joachim
    Harder, Juergen
    Schroeder, Jens-M.
    [J]. DEVELOPMENTAL AND COMPARATIVE IMMUNOLOGY, 2009, 33 (04) : 559 - 569
  • [10] Maternal transfer of antibodies: raising immuno-ecology issues
    Boulinier, Thierry
    Staszewski, Vincent
    [J]. TRENDS IN ECOLOGY & EVOLUTION, 2008, 23 (05) : 282 - 288