Abstract
For a microbial association to persist throughout generations, host progeny must either be capable of earning a microbial fortune from the environment (horizontal transmission) or inherit it from its parents (vertical transmission). The former modality relies on highly sophisticated molecular mechanisms of partners’ recognition. The latter modality, instead, presupposes the microbial partners to be as deeply integrated into the host life cycle and to associate with its earliest developmental stages. Besides the common trends that just started to emerge, I discuss the under-explored aspects of bacterial transmission such as its cell biology, and how extracellular microbial symbionts – in turn – ensure their daughter cells the symbiotic lifestyle.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Albertson R, Doe CQ (2003) Dlg, Scrib and Lgl regulate neuroblast cell size and mitotic spindle asymmetry. Nat Cell Biol 5(2):166–170
Albertson R, Casper-Lindley C et al (2009) Symmetric and asymmetric mitotic segregation patterns influence Wolbachia distribution in host somatic tissue. J Cell Sci 122(Pt 24):4570–4583
Angert ER (2005) Alternatives to binary fission in bacteria. Nat Rev Microbiol 3(3):214–224
Angert ER, Losick RM (1998) Propagation by sporulation in the guinea pig symbiont Metabacterium polyspora. Proc Natl Acad Sci USA 95(17):10218–10223
Bayer C, Heindl NR et al (2009) Molecular characterization of the symbionts associated with marine nematodes of the genus Robbea. Environ Microbiol Rep 1(2):136–144
Bazzocchi C, Comazzi S et al (2007) Wolbachia surface protein (WSP) inhibits apoptosis in human neutrophils. Parasite Immunol 29(2):73–79
Braendle C, Miura T et al (2003) Developmental origin and evolution of bacteriocytes in the aphid-Buchnera symbiosis. PLoS Biol 1(1):E21
Brattig NW, Bazzocchi C et al (2004) The major surface protein of Wolbachia endosymbionts in filarial nematodes elicits immune responses through TLR2 and TLR4. J Immunol 173(1):437–445
Bright M, Bulgheresi S (2010) A complex journey: transmission of microbial symbionts. Nat Rev Microbiol 8(3):218–230
Bright M, Giere O (2005) Microbial symbiosis in Annelida. Symbiosis 38(1):1–45
Chase DG, Erlandsen SL (1976) Evidence for a complex life cycle and endospore formation in the attached, filamentous, segmented bacterium from murine ileum. J Bacteriol 127(1):572–583
Chaston J, Goodrich-Blair H (2010) Common trends in mutualism revealed by model associations between invertebrates and bacteria. FEMS Microbiol Rev 34(1):41–58
Clements KD (1997) Fermentation and gastrointestinal microorganisms of fishes. In: Mackie RI, White BA (eds) Gastrointestinal microbiology: gastrointestinal ecosystems and fermentations, vol 1. Chapman and Hall, New York, pp 156–198
Cowles CE, Goodrich-Blair H (2004) Characterization of a lipoprotein, NilC, required by Xenorhabdus nematophila for mutualism with its nematode host. Mol Microbiol 54(2):464–477
Cowles CE, Goodrich-Blair H (2008) The Xenorhabdus nematophila nilABC genes confer the ability of Xenorhabdus spp. to colonize Steinernema carpocapsae nematodes. J Bacteriol 190(12):4121–4128
Davis CP, Savage DC (1974) Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract. Infect Immun 10(4):948–956
De Mita S, Santoni S et al (2006) Molecular evolution and positive selection of the symbiotic gene NORK in Medicago truncatula. J Mol Evol 62(2):234–244
De Mita S, Ronfort J et al (2007) Investigation of the demographic and selective forces shaping the nucleotide diversity of genes involved in nod factor signaling in Medicago truncatula. Genetics 177(4):2123–2133
Dobson SL (2003) Reversing Wolbachia-based population replacement. Trends Parasitol 19(3):128–133
Erlandsen SL, Chase DG (1974) Morphological alterations in the microvillous border of villous epithelial cells produced by intestinal microorganisms. Am J Clin Nutr 27(11):1277–1286
Faucher C, Maillet F et al (1988) Rhizobium meliloti host range nodH gene determines production of an alfalfa-specific extracellular signal. J Bacteriol 170(12):5489–5499
Fenchel T, Finlay BJ (1989) Kentrophoros: a mouthless ciliate with a symbiotic kitchen garden. Ophelia 30:75–93
Fuller MT, Spradling AC (2007) Male and female Drosophila germline stem cells: two versions of immortality. Science 316(5823):402–404
Giere O, Krieger J (2001) A triple bacterial endosymbiosis in a gutless oligochaete (Annelida): ultrastructural and immunocytochemical evidence. Invert Biol 120(1):41–49
Goldstein B, Macara IG (2007) The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13(5):609–622
Goodman CS, Doe CQ (1993) Embryonic development of the drosophila central nervous system. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Gourdine JP, Smith-Ravin EJ (2007) Analysis of a cDNA-derived sequence of a novel mannose-binding lectin, codakine, from the tropical clam Codakia orbicularis. Fish Shellfish Immunol 22(5):498–509
Hinnebusch BJ, Rudolph AE et al (2002) Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296(5568):733–735
Kaltschmidt JA, Davidson CM et al (2000) Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nat Cell Biol 2(1):7–12
Klaasen HL, Koopman JP et al (1993) Intestinal, segmented, filamentous bacteria in a wide range of vertebrate species. Lab Anim 27(2):141–150
Kraut R, Chia W et al (1996) Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature 383(6595):50–55
Kvennefors EC, Leggat W et al (2008) An ancient and variable mannose-binding lectin from the coral Acropora millepora binds both pathogens and symbionts. Dev Comp Immunol 32(12):1582–1592
Lambiase S, Grigolo A, Laudani U, Sacchi L, Baccetti B (1997) Pattern of bacteriocyte formation in Periplaneta americana (L.) (Blattaria: Blattidae). Int J Insect Morphol Embryol 26:9–19
Landmann F, Foster JM et al (2010) Asymmetric Wolbachia segregation during early Brugia malayi embryogenesis determines its distribution in adult host tissues. PLoS Negl Trop Dis 4(7):e758
Mandel MJ (2010) Models and approaches to dissect host-symbiont specificity. Trends Microbiol 18(11):504–511
Mandel MJ, Wollenberg MS et al (2009) A single regulatory gene is sufficient to alter bacterial host range. Nature 458(7235):215–218
Masson-Boivin C, Giraud E et al (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol 17(10):458–466
McAuley PJ (1982) Temporal relationships of host cell and algal mitosis in the green hydra symbiosis. J Cell Sci 58:423–431
Mira A, Ochman H et al (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17(10):589–596
Miura T, Braendle C et al (2003) A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). J Exp Zool B Mol Dev Evol 295(1):59–81
Moran NA, Plague GR (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14(6):627–633
Moran NA, McCutcheon JP et al (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190
Moran NA, McLaughlin HJ et al (2009) The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323(5912):379–382
Niki Y, Yamaguchi T et al (2006) Establishment of stable cell lines of Drosophila germ-line stem cells. Proc Natl Acad Sci USA 103(44):16325–16330
Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546
Ott JA, Bright M et al (2004a) Marine microbial thiotrophic ectosymbioses. Oceanogr Mar Biol Annu Rev 42:95–118
Ott JA, Bright M et al (2004b) Symbioses between marine nematodes and sulfur-oxidizing chemoautotrophic bacteria. Symbiosis 36(2):103–126
Pflugfelder B, Cary SC et al (2009) Dynamics of cell proliferation and apoptosis reflect different life strategies in hydrothermal vent and cold seep vestimentiferan tubeworms. Cell Tissue Res 337(1):149–165
Polz MF, Distel DL et al (1994) Phylogenetic analysis of a highly specific association between ectosymbiotic, sulfur-oxidizing bacteria and a marine nematode. Appl Environ Microbiol 60(12):4461–4467
Porksakorn C, Nuchprayoon S et al (2007) Proinflammatory cytokine gene expression by murine macrophages in response to Brugia malayi Wolbachia surface protein. Mediators Inflamm 2007:84318
Roche P, Debelle F et al (1991) Molecular basis of symbiotic host specificity in Rhizobium meliloti: nodH and nodPQ genes encode the sulfation of lipo-oligosaccharide signals. Cell 67(6):1131–1143
Sachs JL, Essenberg CJ et al (2011) New paradigms for the evolution of beneficial infections. Trends Ecol Evol 26(4):202–209
Schwarz JA, Brokstein PB et al (2008) Coral life history and symbiosis: functional genomic resources for two reef building Caribbean corals, Acropora palmata and Montastraea faveolata. BMC Genomics 9:97
Serbus LR, Sullivan W (2007) A cellular basis for Wolbachia recruitment to the host germline. PLoS Pathog 3(12):e190
Serbus LR, Casper-Lindley C et al (2008) The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42:683–707
Strassert JF, Desai MS et al (2009) The true diversity of devescovinid flagellates in the termite Incisitermes marginipennis. Protist 160(4):522–535
Wier AM, Nyholm SV et al (2010) Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc Natl Acad Sci USA 107(5):2259–2264
Zielinski FU, Pernthaler A et al (2009) Widespread occurrence of an intranuclear bacterial parasite in vent and seep bathymodiolin mussels. Environ Microbiol 11(5):1150–1167
Acknowledgments
I would like to thank Monika Bright, Ulrich Dirks, Salvador Espada, Harald R. Gruber-Vodicka, Niels R. Heindl, Wolfgang Miller, and Joerg A. Ott for inspiring discussions. The author was supported by the Austrian Science Fund (FWF) project P22470.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Bulgheresi, S. (2012). Microbial Symbiont Transmission: Basic Principles and Dark Sides. In: Rosenberg, E., Gophna, U. (eds) Beneficial Microorganisms in Multicellular Life Forms. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-21680-0_22
Download citation
DOI: https://doi.org/10.1007/978-3-642-21680-0_22
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-21679-4
Online ISBN: 978-3-642-21680-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)