Modelled microgravity impacts Vibrio fischeri population structure in a mutualistic association with an animal host.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
12 Oct 2023
12 Oct 2023
Historique:
received:
04
04
2023
accepted:
28
09
2023
medline:
13
10
2023
pubmed:
13
10
2023
entrez:
12
10
2023
Statut:
aheadofprint
Résumé
Perturbations to host-microbe interactions, such as environmental stress, can alter and disrupt homeostasis. In this study, we examined the effects of a stressor, simulated microgravity, on beneficial bacteria behaviours when colonising their host. We studied the bacterium Vibrio fischeri, which establishes a mutualistic association in a symbiosis-specific organ within the bobtail squid, Euprymna scolopes. To elucidate how animal-microbe interactions are affected by the stress of microgravity, squid were inoculated with different bacterial strains exhibiting either a dominant- or sharing-colonisation behaviour in High Aspect Ratio Vessels, which simulate the low-shear environment of microgravity. The colonisation behaviours of the sharing and dominant strains under modelled microgravity conditions were determined by counting light-organ homogenate of squids as well as confocal microscopy to assess the partitioning of different strains within the light organ. The results indicated that although the colonisation behaviours of the strains did not change, the population levels of the sharing strains were at lower relative abundance in single-colonised animals exposed to modelled microgravity compared to unit gravity; in addition, there were shifts in the relative abundance of strains in co-colonised squids. Together these results suggest that the initiation of beneficial interactions between microbes and animals can be altered by environmental stress, such as simulated microgravity.
Identifiants
pubmed: 37828645
doi: 10.1111/1462-2920.16522
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NASA
ID : 80NSSC18K1465
Pays : United States
Organisme : NASA
ID : 80NSSC19K0138
Pays : United States
Informations de copyright
© 2023 Applied Microbiology International and John Wiley & Sons Ltd.
Références
Abbo, L.A., Himebaugh, N.E., DeMelo, L.M., Hanlon, R.T. & Crook, R.J. (2021) Anesthetic efficacy of magnesium chloride and ethyl alcohol in temperate octopus and cuttlefish species. Journal of the American Association for Laboratory Animal Science, 60, 556-567.
Altura, M.A., Heath-Heckman, E.A., Gillette, A., Kremer, N., Krachler, A.M., Brennan, C. et al. (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. Environmental Microbiology, 15, 2937-2950.
Anderson, K.E., Rodrigues, P.A., Mott, B.M., Maes, P. & Corby-Harris, V. (2016) Ecological succession in the honey bee gut: shift in Lactobacillus strain dominance during early adult development. Microbial Ecology, 71, 1008-1019.
Bizzarri, M., Cucina, A., Palombo, A. & Masiello, M.G. (2014) Gravity sensing by cells: mechanisms and theoretical grounds. Rendiconti Lincei, 25, 29-38.
Boettcher, K.J. & Ruby, E.G. (1990) Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. Journal of Bacteriology, 172, 3701-3706.
Bongrand, C., Koch, E.J., Moriano-Gutierrez, S., Cordero, O.X., McFall-Ngai, M., Polz, M.F. et al. (2016) A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior. The ISME Journal, 10, 2907-2917.
Bongrand, C., Moriano-Gutierrez, S., Arevalo, P., McFall-Ngai, M., Visick, K.L., Polz, M. et al. (2020) Using colonization assays and comparative genomics to discover Symbiosis behaviors and factors in Vibrio fischeri. MBio, 11, 11.
Bongrand, C. & Ruby, E.G. (2019a) The impact of Vibrio fischeri strain variation on host colonization. Current Opinion in Microbiology, 50, 15-19.
Bongrand, C. & Ruby, E.G. (2019b) Achieving a multi-strain symbiosis: strain behavior and infection dynamics. The ISME Journal, 13, 698-706.
Casaburi, G., Goncharenko-Foster, I., Duscher, A.A. & Foster, J.S. (2017) Transcriptomic changes in an animal-bacterial symbiosis under modeled microgravity conditions. Scientific Reports, 7, 46318.
Devevey, G., Dang, T., Graves, C.J., Murray, S. & Brisson, D. (2015) First arrived takes all: inhibitory priority effects dominate competition between co-infecting Borrelia burgdorferi strains. BMC Microbiology, 15, 61.
Drew, G.C. & King, K.C. (2022) More or less? The effect of symbiont density in protective mutualisms. American Naturalist, 199, 443-454.
Dunn, A.K., Millikan, D.S., Adin, D.M., Bose, J.L. & Stabb, E.V. (2006) New rfp- and pES213-derived tools for analyzing symbiotic Vibrio fischeri reveal patterns of infection and lux expression in situ. Applied and Environmental Microbiology, 72, 802-810.
Duscher, A.A., Conesa, A., Bishop, M., Vroom, M.M., Zubizarreta, S.D. & Foster, J.S. (2018) Transcriptional profiling of the mutualistic bacterium Vibrio fischeri and an hfq mutant under modeled microgravity. npj Microgravity, 4, 25.
Ellegaard, K.M. & Engel, P. (2019) Genomic diversity landscape of the honey bee gut microbiota. Nature Communications, 10, 446.
Essock-Burns, T., Bongrand, C., Goldman, W.E., Ruby, E.G. & McFall-Ngai, M.J. (2020) Interactions of symbiotic partners drive the development of a complex biogeography in the squid-vibrio Symbiosis. MBio, 11, 11.
Fiorito, G., Affuso, A., Basil, J., Cole, A., de Girolamo, P., D'Angelo, L. et al. (2015) Guidelines for the care and welfare of cephalopods in research-a consensus based on an initiative by CephRes, FELASA and the Boyd Group. Laboratory Animals, 49, 1-90.
Foster, J.S., Khodadad, C.L., Ahrendt, S.R. & Parrish, M.L. (2013) Impact of simulated microgravity on the normal developmental time line of an animal-bacterial symbiosis. Scientific Reports, 3, 1340.
Garrett-Bakelman, F.E., Darshi, M., Green, S.J., Gur, R.C., Lin, L., Macias, B.R. et al. (2019) The NASA twins study: a multidimensional analysis of a year-long human spaceflight. Science, 364, eaau8650.
Gilarranz, L.J., Rayfield, B., Liñán-Cembrano, G., Bascompte, J. & Gonzalez, A. (2017) Effects of network modularity on the spread of perturbation impact in experimental metapopulations. Science (New York, N.Y.), 357, 199-201.
Gilbert, R., Torres, M., Clemens, R., Hateley, S., Hosamani, R., Wade, W. et al. (2020) Spaceflight and simulated microgravity conditions increase virulence of Serratia marcescens in the Drosophila melanogaster infection model. npj Microgravity, 6, 4.
Grant, K.A., Khodadad, C.L. & Foster, J.S. (2014) Role of Hfq in an animal-microbe symbiosis under simulated microgravity conditions. International Journal of Astrobiology, 13, 53-61.
Hariom, S.K., Ravi, A., Mohan, G.R. & Porchiraju, H.D. (2021) Animal physiology across the gravity continuum. Acta Astronautica, 178, 522-535.
Hodgson, D.J., Rainey, P.B. & Buckling, A. (2002) Mechanisms linking diversity, productivity and invasibility in experimental bacterial communities. Proceedings of the Biological Sciences, 269, 2277-2283.
Kim, W., Tengra, F.K., Young, Z., Shong, J., Marchand, N., Chan, H.K. et al. (2013) Spaceflight promotes biofilm formation by Pseudomonas aeruginosa. PLoS One, 8, e62437.
Koehler, S., Gaedeke, R., Thompson, C., Bongrand, C., Visick, K.L., Ruby, E. et al. (2019) The model squid-vibrio symbiosis provides a window into the impact of strain- and species-level differences during the initial stages of symbiont engagement. Environmental Microbiology, 21, 3269-3283.
Lee, K.H. & Ruby, E.G. (1994) Competition between Vibrio fischeri strains during initiation and maintenance of a light organ symbiosis. Journal of Bacteriology, 176, 1985-1991.
Lee, K.W., Periasamy, S., Mukherjee, M., Xie, C., Kjelleberg, S. & Rice, S.A. (2014) Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. The ISME Journal, 8, 894-907.
Mandel, M.J., Stabb, E.V. & Ruby, E.G. (2008) Comparative genomics-based investigation of resequencing targets in Vibrio fischeri: focus on point miscalls and artefactual expansions. BMC Genomics, 9, 138.
Mandel, M.J., Wollenberg, M.S., Stabb, E.V., Visick, K.L. & Ruby, E.G. (2009) A single regulatory gene is sufficient to alter bacterial host range. Nature, 458, 215-218.
Marsden, A.E., Grudzinski, K., Ondrey, J.M., DeLoney-Marino, C.R. & Visick, K.L. (2017) Impact of salt and nutrient content on biofilm formation by Vibrio fischeri. PLoS One, 12, e0169521.
McCann, J., Stabb, E.V., Millikan, D.S. & Ruby, E.G. (2003) Population dynamics of Vibrio fischeri during infection of Euprymna scolopes. Applied and Environmental Microbiology, 69, 5928-5934.
McFall-Ngai, M., Nyholm, S.V. & Castillo, M.G. (2010) The role of the immune system in the initiation and persistence of the Euprymna scolopes-Vibrio fischeri symbiosis. Seminars in Immunology, 22, 48-53.
McFall-Ngai, M. & Ruby, E. (2021) Getting the message out: the many modes of host-symbiont communication during early-stage establishment of the squid-vibrio partnership. mSystems, 6, e0086721.
Montgomery, M.K. & McFall-Ngai, M. (1993) Embryonic development of the light organ of the sepiolid squid Euprymna scolopes berry. The Biological Bulletin, 184, 296-308.
Mora, M., Wink, L., Kogler, I., Mahnert, A., Rettberg, P., Schwendner, P. et al. (2019) Space station conditions are selective but do not alter microbial characteristics relevant to human health. Nature Communications, 10, 3990.
Morrissey, K.L., Ivesa, L., Delva, S., D'Hondt, S., Willems, A. & De Clerck, O. (2021) Impacts of environmental stress on resistance and resilience of algal-associated bacterial communities. Ecology and Evolution, 11, 15004-15019.
Nawroth, J.C., Guo, H., Koch, E., Heath-Heckman, E.A.C., Hermanson, J.C., Ruby, E.G. et al. (2017) Motile cilia create fluid-mechanical microhabitats for the active recruitment of the host microbiome. Proceedings of the National Academy of Sciences of the United States of America, 114, 9510-9516.
Nyholm, S.V., Stabb, E.V., Ruby, E.G. & McFall-Ngai, M.J. (2000) Establishment of an animal-bacterial association: recruiting symbiotic vibrios from the environment. Proceedings of the National Academy of Sciences of the United States of America, 97, 10231-10235.
Polzin, J., Arevalo, P., Nussbaumer, T., Polz, M.F. & Bright, M. (2019) Polyclonal symbiont populations in hydrothermal vent tubeworms and the environment. Proceedings of the Biological Sciences, 286, 20181281.
Raina, J.B., Fernandez, V., Lambert, B., Stocker, R. & Seymour, J.R. (2019) The role of microbial motility and chemotaxis in symbiosis. Nature Reviews. Microbiology, 17, 284-294.
Rotman, E.R., Bultman, K.M., Brooks, J.F., 2nd, Gyllborg, M.C., Burgos, H.L., Wollenberg, M.S. et al. (2019) Natural strain variation reveals diverse biofilm regulation in squid-colonizing Vibrio fischeri. Journal of Bacteriology, 201, e00033-19.
Ruby, E.G. & McFall-Ngai, M.J. (1992) A squid that glows in the night: development of an animal-bacterial mutualism. Journal of Bacteriology, 174, 4865-4870.
Schlomann, B.H., Wiles, T.J., Wall, E.S., Guillemin, K. & Parthasarathy, R. (2018) Bacterial cohesion predicts spatial distribution in the larval zebrafish intestine. Biophysics Journal, 115, 2271-2277.
Schwarz, R.P., Goodwin, T.J. & Wolf, D.A. (1992) Cell culture for three-dimensional modeling in rotating-wall vessels: an application of simulated microgravity. Journal of Tissue Culture Methods, 14, 51-58.
Shibata, S., Yip, E.S., Quirke, K.P., Ondrey, J.M. & Visick, K.L. (2012) Roles of the structural symbiosis polysaccharide (syp) genes in host colonization, biofilm formation, and polysaccharide biosynthesis in Vibrio fischeri. Journal of Bacteriology, 194, 6736-6747.
Speare, L., Cecere, A.G., Guckes, K.R., Smith, S., Wollenberg, M.S., Mandel, M.J. et al. (2018) Bacterial symbionts use a type VI secretion system to eliminate competitors in their natural host. Proceedings of the National Academy of Sciences of the United States of America, 115, E8528-E8537.
Su, X., Guo, Y., Fang, T., Jiang, X., Wang, D., Li, D. et al. (2021) Effects of simulated microgravity on the physiology of Stenotrophomonas maltophilia and multiomic analysis. Frontiers in Microbiology, 12, 701265.
Sycuro, L.K., Ruby, E.G. & McFall-Ngai, M. (2006) Confocal microscopy of the light organ crypts in juvenile Euprymna scolopes reveals their morphological complexity and dynamic function in symbiosis. Journal of Morphology, 267, 555-568.
Tischler, A.H., Lie, L., Thompson, C.M. & Visick, K.L. (2018) Discovery of calcium as a biofilm-promoting signal for Vibrio fischeri reveals new phenotypes and underlying regulatory complexity. Journal of Bacteriology, 200, e000016-18.
Todd, P. (1989) Gravity-dependent phenomena at the scale of the single cell. ASGSB Bulletin, 2, 95-113.
Van Rossum, T., Ferretti, P., Maistrenko, O.M. & Bork, P. (2020) Diversity within species: interpreting strains in microbiomes. Nature Reviews. Microbiology, 18, 491-506.
Vatanen, T., Franzosa, E.A., Schwager, R., Tripathi, S., Arthur, T.D., Vehik, K. et al. (2018) The human gut microbiome in early-onset type 1 diabetes from the TEDDY study. Nature, 562, 589-594.
Visick, K.L. (2009) An intricate network of regulators controls biofilm formation and colonization by Vibrio fischeri. Molecular Microbiology, 74, 782-789.
Visick, K.L., Stabb, E.V. & Ruby, E.G. (2021) A lasting symbiosis: how Vibrio fischeri finds a squid partner and persists within its natural host. Nature Reviews. Microbiology, 19, 654-665.
Vroom, M.M., Rodriguez-Ocasio, Y., Lynch, J.B., Ruby, E.G. & Foster, J.S. (2021) Modeled microgravity alters lipopolysaccharide and outer membrane vesicle production of the beneficial symbiont Vibrio fischeri. npj Microgravity, 7, 8.
Vroom, M.M., Troncoso-Garcia, A., Duscher, A.A. & Foster, J.S. (2022) Modeled microgravity alters apoptotic gene expression and caspase activity in the squid-vibrio symbiosis. BMC Microbiology, 22, 202.
Wolf, D.A. & Schwarz, R.P. (1991) Analysis of gravity-induced particle motion and fluid perfusion flow in NASA-designed rotating zero-head-space tissue culture vessel. NASA Technical Paper, 3143, 1-12.
Wollenberg, M.S. & Ruby, E.G. (2009) Population structure of Vibrio fischeri within the light organs of Euprymna scolopes squid from two Oahu (Hawaii) populations. Applied and Environmental Microbiology, 75, 193-202.
Wollenberg, M.S. & Ruby, E.G. (2012) Phylogeny and fitness of Vibrio fischeri from the light organs of Euprymna scolopes in two Oahu, Hawaii populations. The ISME Journal, 6, 352-362.
Yip, E.S., Geszvain, K., DeLoney-Marino, C.R. & Visick, K.L. (2006) The symbiosis regulator rscS controls the syp gene locus, biofilm formation and symbiotic aggregation by Vibrio fischeri. Molecular Microbiology, 62, 1586-1600.