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Fiat Lux: The Squid–Vibrio Association as a Model for Understanding Host–Microbe Associations

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The Mechanistic Benefits of Microbial Symbionts

Part of the book series: Advances in Environmental Microbiology ((AEM,volume 2))

Abstract

The symbiosis between the Hawaiian bobtail squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri offers an experimentally tractable model for understanding the role of beneficial bacteria on animal development and the mechanisms by which host and symbionts establish and maintain highly specific associations. The symbiont is transmitted from the environment each generation, and mechanisms must be in place to ensure specificity. Research over the years has revealed some of the “molecular dialogue” that occurs between the partners during and after colonization. Many of these interactions involve microbe-associated molecular patterns (MAMPs) and host pattern recognition receptors (PRRs) as well as components of the host’s innate immune system. The role of light production by the symbiont and light detection by the host is also critical to the association and has likely served as a driving force during the evolution of this symbiosis. Finally, the host harbors a second symbiosis, housing a consortium of bacteria in the female reproductive system. Euprymna scolopes therefore offers the unique opportunity to study both a binary and consortial symbiosis in the same host.

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References

  • Albertin CB, Bonnaud L, Brown CT, Crookes-Goodson WJ, da Fonseca RR, Di Cristo C, Dilkes BP, Edsinger-Gonzales E, Freeman RM Jr, Hanlon RT, Koenig KM, Lindgren AR, Martindale MQ, Minx P, Moroz LL, Nodl MT, Nyholm SV, Ogura A, Pungor JR, Rosenthal JJ, Schwarz EM, Shigeno S, Strugnell JM, Wollesen T, Zhang G, Ragsdale CW (2012) Cephalopod genomics: a plan of strategies and organization. Stand Genomic Sci 7(1):175–188. doi:10.4056/sigs.3136559

    Article  PubMed  PubMed Central  Google Scholar 

  • Altura MA, Stabb E, Goldman W, Apicella M, McFall-Ngai MJ (2011) Attenuation of host NO production by MAMPs potentiates development of the host in the squid-vibrio symbiosis. Cell Microbiol 13(4):527–537. doi:10.1111/j.1462-5822.2010.01552.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altura MA, Heath-Heckman EA, Gillette A, Kremer N, Krachler AM, Brennan C, Ruby EG, Orth K, McFall-Ngai MJ (2013) The first engagement of partners in the Euprymna scolopes-Vibrio fischeri symbiosis is a two-step process initiated by a few environmental symbiont cells. Environ Microbiol. doi:10.1111/1462-2920.12179

    PubMed  PubMed Central  Google Scholar 

  • Barbieri E, Paster BJ, Hughes D, Zurek L, Moser DP, Teske A, Sogin ML (2001) Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda:Loliginidae). Environ Microbiol 3(3):151–167

    Article  CAS  PubMed  Google Scholar 

  • Bloodgood RA (1977) The squid accessory nidamental gland: ultrastructure and association with bacteria. Tissue Cell 9(2):197–208

    Article  CAS  PubMed  Google Scholar 

  • Boettcher KJ, Ruby EG, McFall-Ngai MJ (1996) Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J Comp Physiol 179:65–73

    Article  Google Scholar 

  • Brennan CA, Mandel MJ, Gyllborg MC, Thomasgard KA, Ruby EG (2013) Genetic determinants of swimming motility in the squid light-organ symbiont Vibrio fischeri. Microbiologyopen 2(4):576–594. doi:10.1002/mbo3.96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo MG, Goodson MS, McFall-Ngai M (2009) Identification and molecular characterization of a complement C3 molecule in a lophotrochozoan, the Hawaiian bobtail squid Euprymna scolopes. Dev Comp Immunol 33(1):69–76. doi:10.1016/j.dci.2008.07.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chun CK, Troll JV, Koroleva I, Brown B, Manzella L, Snir E, Almabrazi H, Scheetz TE, Bonaldo Mde F, Casavant TL, Soares MB, Ruby EG, McFall-Ngai MJ (2008) Effects of colonization, luminescence, and autoinducer on host transcription during development of the squid-vibrio association. Proc Natl Acad Sci USA 105(32):11323–11328. doi:10.1073/pnas.0802369105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins AJ, LaBarre BA, Won BS, Shah MV, Heng S, Choudhury MH, Haydar SA, Santiago J, Nyholm SV (2012a) Diversity and partitioning of bacterial populations within the accessory nidamental gland of the squid Euprymna scolopes. Appl Environ Microbiol 78(12):4200–4208. doi:10.1128/AEM.07437-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collins AJ, Schleicher TR, Rader BA, Nyholm SV (2012b) Understanding the role of host hemocytes in a squid/vibrio symbiosis using transcriptomics and proteomics. Front Immunol 3:91. doi:10.3389/fimmu.2012.00091

    Article  PubMed  PubMed Central  Google Scholar 

  • Davidson SK, Koropatnick TA, Kossmehl R, Sycuro L, McFall-Ngai MJ (2004) NO means ‘yes’ in the squid-vibrio symbiosis: nitric oxide (NO) during the initial stages of a beneficial association. Cell Microbiol 6(12):1139–1151. doi:10.1111/j.1462-5822.2004.00429.x

    Article  CAS  PubMed  Google Scholar 

  • Deloney-Marino CR, Visick KL (2012) Role for cheR of Vibrio fischeri in the Vibrio-squid symbiosis. Can J Microbiol 58(1):29–38. doi:10.1139/W11-107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DeLoney-Marino CR, Wolfe AJ, Visick KL (2003) Chemoattraction of Vibrio fischeri to serine, nucleosides, and N-acetylneuraminic acid, a component of squid light-organ mucus. Appl Environ Microbiol 69(12):7527–7530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doino J, McFall-Ngai MJ (1995) A transient exposure to symbiosis-competent bacteria induces light organ morphogenesis in the host squid. Biol Bull 189:347–355

    Article  Google Scholar 

  • Dubilier N, Bergin C, Lott C (2008) Symbiotic diversity in marine animals: the art of harnessing chemosynthesis. Nat Rev Microbiol 6(10):725–740. doi:10.1038/nrmicro1992

    Article  CAS  PubMed  Google Scholar 

  • Dunn AK, Karr EA, Wang Y, Batton AR, Ruby EG, Stabb EV (2010) The alternative oxidase (AOX) gene in Vibrio fischeri is controlled by NsrR and upregulated in response to nitric oxide. Mol Microbiol 77(1):44–55. doi:10.1111/j.1365-2958.2010.07194.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foster JS, McFall-Ngai MJ (1998) Induction of apoptosis by cooperative bacteria in the morphogenesis of host epithelial tissues. Dev Genes Evol 208(6):295–303

    Article  CAS  PubMed  Google Scholar 

  • Goodson MS, Kojadinovic M, Troll JV, Scheetz TE, Casavant TL, Soares MB, McFall-Ngai MJ (2005) Identifying components of the NF-kappaB pathway in the beneficial Euprymna scolopes-Vibrio fischeri light organ symbiosis. Appl Environ Microbiol 71(11):6934–6946. doi:10.1128/AEM.71.11.6934-6946.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graf J, Dunlap PV, Ruby EG (1994) Effect of transposon-induced motility mutations on colonization of the host light organ by Vibrio fischeri. J Bacteriol 176(22):6986–6991

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gray KM, Greenberg EP (1992) Physical and functional maps of the luminescence gene cluster in an autoinducer-deficient Vibrio fischeri strain isolated from a squid light organ. J Bacteriol 174(13):4384–4390

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guerrero-Ferreira RC, Nishiguchi MK (2007) Biodiversity among luminescent symbionts from squid of the genera Uroteuthis, Loliolus and Euprymna (Mollusca: Cephalopoda). Cladistics 23(5):497–506. doi:10.1111/j.1096-0031.2007.00155.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Guerrero-Ferreira R, Gorman C, Chavez AA, Willie S, Nishiguchi MK (2013) Characterization of the bacterial diversity in Indo-West Pacific loliginid and sepiolid squid light organs. Microb Ecol 65(1):214–226. doi:10.1007/s00248-012-0099-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanlon RT, Claes MF, Ashcraft SE, Dunlap PV (1997) Laboratory culture of the sepiolid squid Euprymna scolopes: a model system for bacteria-animal symbiosis. Biol Bull 192:364–374

    Article  Google Scholar 

  • Heath-Heckman EA, McFall-Ngai MJ (2011) The occurrence of chitin in the hemocytes of invertebrates. Zoology (Jena) 114(4):191–198. doi:10.1016/j.zool.2011.02.002

    Article  Google Scholar 

  • Heath-Heckman EA, Peyer SM, Whistler CA, Apicella MA, Goldman WE, McFall-Ngai MJ (2013) Bacterial bioluminescence regulates expression of a host cryptochrome gene in the squid-Vibrio symbiosis. mBio 4(2). doi:10.1128/mBio.00167-13

  • Heath-Heckman EA, Gillette AA, Augustin R, Gillette MX, Goldman WE, McFall-Ngai MJ (2014) Shaping the microenvironment: evidence for the influence of a host galaxin on symbiont acquisition and maintenance in the squid-vibrio symbiosis. Environ Microbiol. doi:10.1111/1462-2920.12496

    PubMed  PubMed Central  Google Scholar 

  • Hussa EA, O’Shea TM, Darnell CL, Ruby EG, Visick KL (2007) Two-component response regulators of Vibrio fischeri: identification, mutagenesis, and characterization. J Bacteriol 189(16):5825–5838. doi:10.1128/JB.00242-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones BW, Nishiguchi MK (2004) Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes (Mollusca: Cephalopoda). Mar Biol 144:1151–1155

    Article  Google Scholar 

  • Jones BW, Maruyama A, Ouverney CC, Nishiguchi MK (2007) Spatial and temporal distribution of the vibrionaceae in coastal waters of Hawaii, Australia, and France. Microb Ecol 54(2):314–323. doi:10.1007/s00248-006-9204-z

    Article  CAS  PubMed  Google Scholar 

  • Koch EJ, Miyashiro T, McFall-Ngai MJ, Ruby EG (2014) Features governing symbiont persistence in the squid-vibrio association. Mol Ecol 23(6):1624–1634. doi:10.1111/mec.12474

    Article  PubMed  PubMed Central  Google Scholar 

  • Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, McFall-Ngai MJ (2004) Microbial factor-mediated development in a host-bacterial mutualism. Science 306(5699):1186–1188. doi:10.1126/science.1102218

    Article  CAS  PubMed  Google Scholar 

  • Koropatnick TA, Kimbell JR, McFall-Ngai MJ (2007) Responses of host hemocytes during the initiation of the squid-Vibrio symbiosis. Biol Bull 212(1):29–39

    Article  PubMed  Google Scholar 

  • Krasity BC, Troll JV, Weiss JP, McFall-Ngai MJ (2011) LBP/BPI proteins and their relatives: conservation over evolution and roles in mutualism. Biochem Soc Trans 39(4):1039–1044. doi:10.1042/BST0391039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kremer N, Philipp EE, Carpentier MC, Brennan CA, Kraemer L, Altura MA, Augustin R, Hasler R, Heath-Heckman EA, Peyer SM, Schwartzman J, Rader BA, Ruby EG, Rosenstiel P, McFall-Ngai MJ (2013) Initial symbiont contact orchestrates host-organ-wide transcriptional changes that prime tissue colonization. Cell Host Microbe 14(2):183–194. doi:10.1016/j.chom.2013.07.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kremer N, Schwartzman J, Augustin R, Zhou L, Ruby EG, Hourdez S, McFall-Ngai MJ (2014) The dual nature of haemocyanin in the establishment and persistence of the squid-vibrio symbiosis. Proc Biol Sci 281(1785):20140504. doi:10.1098/rspb.2014.0504

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee KH, Ruby EG (1994) Effect of the squid host on the abundance and distribution of symbiotic vibrio fischeri in nature. Appl Environ Microbiol 60(5):1565–1571

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee PN, McFall-Ngai MJ, Callaerts P, de Couet HG (2009) The Hawaiian bobtail squid (Euprymna scolopes): a model to study the molecular basis of eukaryote-prokaryote mutualism and the development and evolution of morphological novelties in cephalopods. Cold Spring Harbor Protocols 2009(11):pdb emo135. doi:10.1101/pdb.emo135

    Google Scholar 

  • Mandel MJ, Wollenberg MS, Stabb EV, Visick KL, Ruby EG (2009) A single regulatory gene is sufficient to alter bacterial host range. Nature 458(7235):215–218. doi:10.1038/nature07660

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandel MJ, Schaefer AL, Brennan CA, Heath-Heckman EA, Deloney-Marino CR, McFall-Ngai MJ, Ruby EG (2012) Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl Environ Microbiol 78(13):4620–4626. doi:10.1128/AEM.00377-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McFall-Ngai M (2014) Divining the essence of symbiosis: insights from the squid-vibrio model. PLoS Biol 12(2):e1001783. doi:10.1371/journal.pbio.1001783

    Article  PubMed  PubMed Central  Google Scholar 

  • McFall-Ngai MJ, Montgomery MK (1990) The anatomy and morphology of the adult bacterial light organ of Euprymna scolopes Berry (Cephalopoda: Sepiolidae). Biol Bull 179:332–339

    Article  Google Scholar 

  • McFall-Ngai MJ, Ruby EG (1991) Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254(5037):1491–1494

    Article  CAS  PubMed  Google Scholar 

  • McFall-Ngai M, Heath-Heckman EA, Gillette AA, Peyer SM, Harvie EA (2012) The secret languages of coevolved symbioses: insights from the Euprymna scolopes-Vibrio fischeri symbiosis. Semin Immunol 24(1):3–8. doi:10.1016/j.smim.2011.11.006

    Article  PubMed  PubMed Central  Google Scholar 

  • McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci USA 110(9):3229–3236. doi:10.1073/pnas.1218525110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Millikan DS, Ruby EG (2002) Alterations in Vibrio fischeri motility correlate with a delay in symbiosis initiation and are associated with additional symbiotic colonization defects. Appl Environ Microbiol 68(5):2519–2528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Millikan DS, Ruby EG (2004) Vibrio fischeri flagellin A is essential for normal motility and for symbiotic competence during initial squid light organ colonization. J Bacteriol 186(13):4315–4325. doi:10.1128/JB.186.13.4315-4325.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miyashiro T, Ruby EG (2012) Shedding light on bioluminescence regulation in Vibrio fischeri. Mol Microbiol 84(5):795–806. doi:10.1111/j.1365-2958.2012.08065.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Montgomery MK, McFall-Ngai M (1994) Bacterial symbionts induce host organ morphogenesis during early postembryonic development of the squid Euprymna scolopes. Development 120(7):1719–1729

    CAS  PubMed  Google Scholar 

  • Norsworthy AN, Visick KL (2013) Gimme shelter: how Vibrio fischeri successfully navigates an animal's multiple environments. Front Microbiol 4:356. doi:10.3389/fmicb.2013.00356

    Article  PubMed  PubMed Central  Google Scholar 

  • Nyholm SV, Graf J (2012) Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses. Nat Rev Microbiol 10(12):815–827. doi:10.1038/nrmicro2894

    Article  CAS  PubMed  Google Scholar 

  • Nyholm SV, McFall-Ngai MJ (1998) Sampling the light-organ microenvironment of Euprymna scolopes: description of a population of host cells in association with the bacterial symbiont Vibrio fischeri. Biol Bull 195(2):89–97

    Article  CAS  PubMed  Google Scholar 

  • Nyholm SV, McFall-Ngai MJ (2003) Dominance of Vibrio fischeri in secreted mucus outside the light organ of Euprymna scolopes: the first site of symbiont specificity. Appl Environ Microbiol 69(7):3932–3937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nyholm SV, McFall-Ngai MJ (2004) The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2(8):632–642. doi:10.1038/nrmicro957

    Article  CAS  PubMed  Google Scholar 

  • Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ (2000) Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci USA 97(18):10231–10235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nyholm SV, Deplancke B, Gaskins HR, Apicella MA, McFall-Ngai MJ (2002) Roles of Vibrio fischeri and nonsymbiotic bacteria in the dynamics of mucus secretion during symbiont colonization of the Euprymna scolopes light organ. Appl Environ Microbiol 68(10):5113–5122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nyholm SV, Stewart JJ, Ruby EG, McFall-Ngai MJ (2009) Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ Microbiol 11(2):483–493. doi:10.1111/j.1462-2920.2008.01788.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Oldroyd GE (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11(4):252–263. doi:10.1038/nrmicro2990

    Article  CAS  PubMed  Google Scholar 

  • Peyer SM, Pankey MS, Oakley TH, McFall-Ngai MJ (2014) Eye-specification genes in the bacterial light organ of the bobtail squid Euprymna scolopes, and their expression in response to symbiont cues. Mech Dev 131:111–126. doi:10.1016/j.mod.2013.09.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rader BA, Nyholm SV (2012) Host/microbe interactions revealed through “omics” in the symbiosis between the Hawaiian bobtail squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri. Biol Bull 223(1):103–111

    CAS  PubMed  Google Scholar 

  • Rader BA, Kremer N, Apicella MA, Goldman WE, McFall-Ngai MJ (2012) Modulation of symbiont lipid A signaling by host alkaline phosphatases in the squid-vibrio symbiosis. mBio 3(3).doi:10.1128/mBio.00093-12

  • Ruby EG (2008) Symbiotic conversations are revealed under genetic interrogation. Nat Rev Microbiol 6(10):752–762. doi:10.1038/nrmicro1958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruby EG, Asato LM (1993) Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch Microbiol 159(2):160–167

    Article  CAS  PubMed  Google Scholar 

  • Schleicher TR, Nyholm SV (2011) Characterizing the host and symbiont proteomes in the association between the Bobtail squid, Euprymna scolopes, and the bacterium, Vibrio fischeri. PLoS One 6(10):e25649. doi:10.1371/journal.pone.0025649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schleicher TR, VerBerkmoes NC, Shah M, Nyholm SV (2014) Colonization state influences the hemocyte proteome in a beneficial squid-vibrio symbiosis. Mol Cell Proteomics. doi:10.1074/mcp.M113.037259

    PubMed  PubMed Central  Google Scholar 

  • Schuster B, Perry L, Cooper V, Whistler C (2010) Breaking the language barrier: experimental evolution of non-native Vibrio fischeri in squid tailors luminescence to the host. Symbiosis 51:72–81

    Article  Google Scholar 

  • Small AL, McFall-Ngai MJ (1999) Halide peroxidase in tissues that interact with bacteria in the host squid Euprymna scolopes. J Cell Biochem 72(4):445–457

    Article  CAS  PubMed  Google Scholar 

  • Soto W, Punke EB, Nishiguchi MK (2012) Evolutionary perspectives in a mutualism of sepiolid squid and bioluminescent bacteria: combined usage of microbial experimental evolution and temporal population genetics. Evolution 66(5):1308–1321. doi:10.1111/j.1558-5646.2011.01547.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tomarev SI, Zinovieva RD, Weis VM, Chepelinsky AB, Piatigorsky J, McFall-Ngai MJ (1993) Abundant mRNAs in the squid light organ encode proteins with a high similarity to mammalian peroxidases. Gene 132(2):219–226

    Article  CAS  PubMed  Google Scholar 

  • Tong D, Rozas NS, Oakley TH, Mitchell J, Colley NJ, McFall-Ngai MJ (2009) Evidence for light perception in a bioluminescent organ. Proc Natl Acad Sci USA 106(24):9836–9841. doi:10.1073/pnas.0904571106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Troll JV, Adin DM, Wier AM, Paquette N, Silverman N, Goldman WE, Stadermann FJ, Stabb EV, McFall-Ngai MJ (2009) Peptidoglycan induces loss of a nuclear peptidoglycan recognition protein during host tissue development in a beneficial animal-bacterial symbiosis. Cell Microbiol 11(7):1114–1127. doi:10.1111/j.1462-5822.2009.01315.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Troll JV, Bent EH, Pacquette N, Wier AM, Goldman WE, Silverman N, McFall-Ngai MJ (2010) Taming the symbiont for coexistence: a host PGRP neutralizes a bacterial symbiont toxin. Environ Microbiol 12(8):2190–2203. doi:10.1111/j.1462-2920.2009.02121.x

    CAS  PubMed  PubMed Central  Google Scholar 

  • Urbanczyk H, Ast JC, Dunlap PV (2011) Phylogeny, genomics, and symbiosis of Photobacterium. FEMS Microbiol Rev 35(2):324–342. doi:10.1111/j.1574-6976.2010.00250.x

    Article  CAS  PubMed  Google Scholar 

  • Verma SC, Miyashiro T (2013) Quorum sensing in the squid-Vibrio symbiosis. Int J Mol Sci 14(8):16386–16401. doi:10.3390/ijms140816386

    Article  PubMed  PubMed Central  Google Scholar 

  • Visick KL, Ruby EG (1998) The periplasmic, group III catalase of Vibrio fischeri is required for normal symbiotic competence and is induced both by oxidative stress and by approach to stationary phase. J Bacteriol 180(8):2087–2092

    CAS  PubMed  PubMed Central  Google Scholar 

  • Visick KL, Foster J, Doino J, McFall-Ngai M, Ruby EG (2000) Vibrio fischeri lux genes play an important role in colonization and development of the host light organ. J Bacteriol 182(16):4578–4586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Ruby EG (2011) The roles of NO in microbial symbioses. Cell Microbiol 13(4):518–526. doi:10.1111/j.1462-5822.2011.01576.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Dunn AK, Wilneff J, McFall-Ngai MJ, Spiro S, Ruby EG (2010) Vibrio fischeri flavohaemoglobin protects against nitric oxide during initiation of the squid-Vibrio symbiosis. Mol Microbiol 78(4):903–915. doi:10.1111/j.1365-2958.2010.07376.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D (2005) Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309(5742):1874–1878. doi:10.1126/science.1116887

    Article  CAS  PubMed  Google Scholar 

  • Weis VM, Small AL, McFall-Ngai MJ (1996) A peroxidase related to the mammalian antimicrobial protein myeloperoxidase in the Euprymna-Vibrio mutualism. Proc Natl Acad Sci USA 93(24):13683–13688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Widder EA (2010) Bioluminescence in the ocean: origins of biological, chemical, and ecological diversity. Science 328(5979):704–708. doi:10.1126/science.1174269

    Article  CAS  PubMed  Google Scholar 

  • Wier AM, Nyholm SV, Mandel MJ, Massengo-Tiasse RP, Schaefer AL, Koroleva I, Splinter-Bondurant S, Brown B, Manzella L, Snir E, Almabrazi H, Scheetz TE, Bonaldo Mde F, Casavant TL, Soares MB, Cronan JE, Reed JL, Ruby EG, McFall-Ngai MJ (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. doi:10.1073/pnas.0909712107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolfe AJ, Millikan DS, Campbell JM, Visick KL (2004) Vibrio fischeri sigma54 controls motility, biofilm formation, luminescence, and colonization. Appl Environ Microbiol 70(4):2520–2524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yip ES, Grublesky BT, Hussa EA, Visick KL (2005) A novel, conserved cluster of genes promotes symbiotic colonization and sigma-dependent biofilm formation by Vibrio fischeri. Mol Microbiol 57(5):1485–1498. doi:10.1111/j.1365-2958.2005.04784.x

    Article  CAS  PubMed  Google Scholar 

  • Yip ES, Geszvain K, DeLoney-Marino CR, Visick KL (2006) The symbiosis regulator rscS controls the syp gene locus, biofilm formation and symbiotic aggregation by Vibrio fischeri. Mol Microbiol 62(6):1586–1600. doi:10.1111/j.1365-2958.2006.05475.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang SM, Adema CM, Kepler TB, Loker ES (2004) Diversification of Ig superfamily genes in an invertebrate. Science 305(5681):251–254. doi:10.1126/science.1088069

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

I would like to thank the numerous collaborators who have contributed to this research, especially the McFall-Ngai and Ruby laboratories at the University of Hawaii. Also, research in the squid–vibrio association would not be possible without the generous support of the Kewalo Marine Laboratory and Hawaii Institute of Marine Biology at the University of Hawaii. I’d like to thank A. Suria for the contribution of drawings of the host and symbiont. This work was funded by NSF IOS 0958006 and the University of Connecticut Research Foundation to SVN.

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  1. University of Connecticut, Storrs, CT, USA

    Spencer V. Nyholm

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  1. Spencer V. Nyholm
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Correspondence to Spencer V. Nyholm .

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  1. Cincinnati, Ohio, USA

    Christon J. Hurst

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Nyholm, S.V. (2016). Fiat Lux: The Squid–Vibrio Association as a Model for Understanding Host–Microbe Associations. In: Hurst, C. (eds) The Mechanistic Benefits of Microbial Symbionts. Advances in Environmental Microbiology, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-319-28068-4_11

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