Many symbiotic relationships rely on the acquisition of microbial partners from the environment. However, the mechanisms by which microbial symbionts find and colonize their hosts are often unknown. We propose that the acquisition of environmental symbionts often necessitates active migration and colonization by the symbionts through motility and chemotaxis. The pivotal role of these behaviours in the onset and maintenance of symbiotic interactions is well established in a small number of model systems but remains largely overlooked for the many symbioses that involve the recruitment of microbial partners from the environment. In this Review, we highlight when, where and how chemotaxis and motility can enable symbiont recruitment and propose that these symbiont behaviours are important across a wide range of hosts and environments.
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Margulis, L. Symbiosis in Cell Evolution: Life and Its Environment on the Early Earth (W. H. Freeman, 1981).
Ochman, H. & Moran, N. A. Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292, 1096–1099 (2001).
Mora, C., Tittensor, D. P., Adl, S., Simpson, A. G. B. & Worm, B. How many species are there on earth and in the ocean? PLOS Biol. 9, e1001127 (2011).
Eme, L., Spang, A., Lombard, J., Stairs, C. W. & Ettema, T. J. G. Archaea and the origin of eukaryotes. Nat. Rev. Microbiol. 15, 711 (2017).
Boucher, D. H., James, S. & Keeler, K. H. The ecology of mutualism. Annu. Rev. Ecol. Syst. 13, 315–347 (1982).
Bright, M. & Bulgheresi, S. A complex journey: transmission of microbial symbionts. Nat. Rev. Microbiol. 8, 218 (2010). This is an important description of the journey undertaken by horizontally and vertically transmitted symbionts, from their initial contact with their host to their final residence.
Bennett, G. M. & Moran, N. A. Heritable symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc. Natl Acad. Sci. USA 112, 10169–10176 (2015).
Bull, J. J., Molineux, I. J. & Rice, W. R. Selection of benevolence in a host-parasite system. Evolution 45, 875–882 (1991).
Doebeli, M. & Knowlton, N. The evolution of interspecific mutualisms. Proc. Natl Acad. Sci. USA USA 95, 8676–8680 (1998).
Douglas, A. E. Host benefit and the evolution of specialization in symbiosis. Heredity 81, 599 (1998).
Ewald, P. W. Transmission modes and evolution of the parasitism-mutualism continuum. Ann. NY Acad. Sci. 503, 295–306 (1987).
Hartmann, A. C., Baird, A. H., Knowlton, N. & Huang, D. The paradox of environmental symbiont acquisition in obligate mutualisms. Curr. Biol. 27, 3711–3716 (2017).
Herre, E. A., Knowlton, N., Mueller, U. G. & Rehner, S. A. The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol. Evol. 14, 49–53 (1999).
Wilkinson, D. M. & Sherratt, T. N. Horizontally acquired mutualisms, an unsolved problem in ecology? Oikos 92, 377–384 (2001).
Knowlton, N. & Rohwer, F. Multispecies microbial mutualisms on coral reefs: the host as a habitat. Am. Nat. 162, S51–S62 (2003).
Nussbaumer, A. D., Fisher, C. R. & Bright, M. Horizontal endosymbiont transmission in hydrothermal vent tubeworms. Nature 441, 345 (2006).
Nyholm, S. V. & McFall-Ngai, M. The winnowing: establishing the squid–vibrio symbiosis. Nat. Rev. Microbiol. 2, 632 (2004). This is a classic overview of the establishment of the squid– Vibrio spp. symbiosis.
Fontanez, K. M. & Cavanaugh, C. M. Evidence for horizontal transmission from multilocus phylogeny of deep-sea mussel (Mytilidae) symbionts. Environ. Microbiol. 16, 3608–3621 (2014).
Oldroyd, G. E. D. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252 (2013). This is an excellent overview of the complex signalling occurring between plants and their symbionts.
Kikuchi, Y., Hosokawa, T. & Fukatsu, T. Insect-microbe mutualism without vertical transmission: a stinkbug acquires a beneficial gut symbiont from the environment every generation. Appl. Environ. Microbiol. 73, 4308–4316 (2007).
Decelle, J. et al. An original mode of symbiosis in open ocean plankton. Proc. Natl Acad. Sci. USA 109, 18000–18005 (2012).
Seymour, J. R., Amin, S. A., Raina, J.-B. & Stocker, R. Zooming in on the phycosphere: the ecological interface for phytoplankton–bacteria relationships. Nat. Microbiol. 2, 17065 (2017).
Böhm, M., Hurek, T. & Reinhold-Hurek, B. Twitching motility is essential for endophytic rice colonization by the N2-fixing endophyte Azoarcus sp. strain BH72. Mol. Plant Microbe Interact. 20, 526–533 (2007).
Geng, H. & Belas, R. Molecular mechanisms underlying roseobacter–phytoplankton symbioses. Curr. Opin. Biotechnol. 21, 332–338 (2010).
Mandel, M. J. et al. Squid-derived chitin oligosaccharides are a chemotactic signal during colonization by Vibrio fischeri. Appl. Environ. Microbiol. 78, 4620–4626 (2012).
Munoz Aguilar, J. M. et al. Chemotaxis of Rhizobium leguminosarum biovar phaseoli towards flavonoid Inducers of the symbiotic nodulation genes. Microbiology 134, 2741–2746 (1988).
Robidart, J. C. et al. Metabolic versatility of the Riftia pachyptila endosymbiont revealed through metagenomics. Environ. Microbiol. 10, 727–737 (2008).
Matilla, M. A. & Krell, T. The effect of bacterial chemotaxis on host infection and pathogenicity. FEMS Microbiol. Rev. 42, fux052 (2018). This is a recent review focusing on the prevalence of chemotaxis in human, animal and plant pathogens.
Moran, N. A., McCutcheon, J. P. & Nakabachi, A. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 42, 165–190 (2008).
Porter, S. L., Wadhams, G. H. & Armitage, J. P. Signal processing in complex chemotaxis pathways. Nat. Rev. Microbiol. 9, 153 (2011).
Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell Biol. 5, 1024 (2004). This is a comprehensive and clearly written review covering the genetic systems involved in bacterial chemotaxis.
Bi, S. & Sourjik, V. Stimulus sensing and signal processing in bacterial chemotaxis. Curr. Opin. Microbiol. 45, 22–29 (2018).
Szurmant, H. & Ordal, G. W. Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol. Mol. Biol. Rev. 68, 301–319 (2004).
Van Haastert, P. J. M. & Devreotes, P. N. Chemotaxis: signalling the way forward. Nat. Rev. Mol. Cell Biol. 5, 626 (2004).
Swaney, K. F., Huang, C.-H. & Devreotes, P. N. Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu. Rev. Biophys. 39, 265–289 (2010).
Berg, H. C. Random Walks in Biology (Princeton Univ. Press, 1993). This is an intuitive reference on the mathematics and biophysics of bacterial motility and chemotaxis.
Leifson, E., Cosenza, B. J., Murchelano, R. & Cleverdon, R. C. Motile marine bacteria. I. Techniques, ecology, and general characteristics. J. Bacteriol. 87, 652–666 (1964).
Xie, L., Altindal, T., Chattopadhyay, S. & Wu, X.-L. Bacterial flagellum as a propeller and as a rudder for efficient chemotaxis. Proc. Natl Acad. Sci. USA 108, 2246–2251 (2011).
Packer, H. L., Lawther, H. & Armitage, J. P. The Rhodobacter sphaeroides flagellar motor is a variable-speed rotor. FEBS Lett. 409, 37–40 (1997).
Son, K., Menolascina, F. & Stocker, R. Speed-dependent chemotactic precision in marine bacteria. Proc. Natl Acad. Sci. USA 113, 8624–8629 (2016).
Takeuchi, R. et al. Establishment of a model for chemoattraction of Symbiodinium and characterization of chemotactic compounds in Acropora tenuis. Fish. Sci. 83, 479–487 (2017).
Sourjik, V. Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol. 12, 569–576 (2004).
Lopez-de-Victoria, G. & Lovell, C. R. Chemotaxis of Azospirillum species to aromatic compounds. Appl. Environ. Microbiol. 59, 2951–2955 (1993).
Bowra, B. J. & Dilworth, M. J. Motility and chemotaxis towards sugars in Rhizobium leguminosarum. Microbiology 126, 231–235 (1981).
Garren, M. et al. A bacterial pathogen uses dimethylsulfoniopropionate as a cue to target heat-stressed corals. ISME J. 8, 999 (2013).
Miller, T. R., Hnilicka, K., Dziedzic, A., Desplats, P. & Belas, R. Chemotaxis of Silicibacter sp. strain TM1040 toward dinoflagellate products. Appl. Environ. Microbiol. 70, 4692–4701 (2004).
Seymour, J. R., Simó, R., Ahmed, T. & Stocker, R. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329, 342–345 (2010).
Adibi, S. A. & Mercer, D. W. Protein digestion in human intestine as reflected in luminal, mucosal, and plasma amino acid concentrations after meals. J. Clin. Invest. 52, 1586–1594 (1973).
Caruana, A. M. N. & Malin, G. The variability in DMSP content and DMSP lyase activity in marine dinoflagellates. Prog. Oceanogr. 120, 410–424 (2014).
Jaeger, C. H., Lindow, S. E., Miller, W., Clark, E. & Firestone, M. K. Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Appl. Environ. Microbiol. 65, 2685–2690 (1999).
Szmant, A. M., Ferrer, L. M. & FitzGerald, L. M. Nitrogen excretion and O:N ratios in reef corals: evidence for conservation of nitrogen. Mar. Biol. 104, 119–127 (1990).
Gage, D. J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68, 280–300 (2004).
Mattick, J. S. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56, 289–314 (2002).
Nan, B. & Zusman, D. R. Novel mechanisms power bacterial gliding motility. Mol. Microbiol. 101, 186–193 (2016).
Kearns, D. B. A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 8, 634 (2010).
Kearns, D. B. & Shimkets, L. J. Chemotaxis in a gliding bacterium. Proc. Natl Acad. Sci. USA 95, 11957–11962 (1998).
Oliveira, N. M., Foster, K. R. & Durham, W. M. Single-cell twitching chemotaxis in developing biofilms. Proc. Natl Acad. Sci. USA 113, 6532–6537 (2016).
Kinosita, Y., Kikuchi, Y., Mikami, N., Nakane, D. & Nishizaka, T. Unforeseen swimming and gliding mode of an insect gut symbiont. Burkholderia sp. RPE64, with wrapping of the flagella around its cell body. ISME J. 12, 838–848 (2018). This paper provides a description of the recently discovered corkscrew motility mode in insect and squid symbionts.
Bakus, G. J., Targett, N. M. & Schulte, B. Chemical ecology of marine organisms: an overview. J. Chem. Ecol. 12, 951–987 (1986).
Crank, J. The Mathematics of Diffusion (Clarendon Press, 1975).
Dulla, G. F. J., Go, R. A., Stahl, D. A. & Davidson, S. K. Verminephrobacter eiseniae type IV pili and flagella are required to colonize earthworm nephridia. ISME J. 6, 1166 (2011).
Mann, K. H. & Lazier, J. R. Dynamics of Marine Ecosystems: Biological-Physical Interactions in the Oceans (John Wiley & Sons, 2013). This oceanography text includes an important chapter on small-scale turbulence and the physics of boundary layers.
Nyholm, S. V., Stabb, E. V., Ruby, E. G. & McFall-Ngai, M. J. Establishment of an animal–bacterial association: recruiting symbiotic vibrios from the environment. Proc. Natl Acad. Sci. USA 97, 10231–10235 (2000).
Taylor, J. R. & Stocker, R. Trade-offs of chemotactic foraging in turbulent water. Science 338, 675–679 (2012). This is a modelling study that illustrates how turbulent fluid motion gives rise to small-scale heterogeneity and chemical gradients.
Guasto, J. S., Rusconi, R. & Stocker, R. Fluid mechanics of planktonic microorganisms. Annu. Rev. Fluid Mech. 44, 373–400 (2012).
Locsei, J. T. & Pedley, T. J. Bacterial tracking of motile algae assisted by algal cell’s vorticity field. Microb. Ecol. 58, 63–74 (2009).
Shapiro, O. H. et al. Vortical ciliary flows actively enhance mass transport in reef corals. Proc. Natl Acad. Sci. USA 111, 13391–13396 (2014).
Vogel, S. Current-induced flow through living sponges in nature. Proc. Natl Acad. Sci. USA 74, 2069–2071 (1977).
Rusconi, R., Guasto, J. S. & Stocker, R. Bacterial transport suppressed by fluid shear. Nat. Physics 10, 212 (2014). This is a study that highlights some of the unexpected dynamics that arise when bacteria are subjected to fluid flows near surfaces.
Lecuyer, S. et al. Shear stress increases the residence time of adhesion of Pseudomonas aeruginosa. Biophys. J. 100, 341–350 (2011).
Fukui, M., Teske, A., Aßmus, B., Muyzer, G. & Widdel, F. Physiology, phylogenetic relationships, and ecology of filamentous sulfate-reducing bacteria (genus Desulfonema). Arch. Microbiol. 172, 193–203 (1999).
Kessler, R. W., Weiss, A., Kuegler, S., Hermes, C. & Wichard, T. Macroalgal–bacterial interactions: role of dimethylsulfoniopropionate in microbial gardening by Ulva (Chlorophyta). Mol. Ecol. 27, 1808–1819 (2018).
Paerl, H. W. & Gallucci, K. K. Role of chemotaxis in establishing a specific nitrogen-fixing cyanobacterial-bacterial association. Science 227, 647–649 (1985).
Sonnenschein, E. C., Abebew Syit, D., Grossart, H.-P. & Ullrich, M. S. Chemotaxis of Marinobacter adhaerens and its impact on attachment to the Diatom Thalassiosira weissflogii. Appl. Environ. Microbiol. 78, 6900–6907 (2012).
Miller, T. R. & Belas, R. Motility is involved in Silicibacter sp. TM1040 interaction with dinoflagellates. Environ. Microbiol. 8, 1648–1659 (2006).
Yamashita, H., Suzuki, G., Kai, S., Hayashibara, T. & Koike, K. Establishment of coral–algal symbiosis requires attraction and selection. PLOS ONE 9, e97003 (2014).
Scharf, B. E., Hynes, M. F. & Alexandre, G. M. Chemotaxis signaling systems in model beneficial plant–bacteria associations. Plant Mol. Biol. 90, 549–559 (2016).
Jones, K. M., Kobayashi, H., Davies, B. W., Taga, M. E. & Walker, G. C. How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model. Nat. Rev. Microbiol. 5, 619 (2007).
Gaworzewska, E. T. & Carlile, M. J. Positive chemotaxis of Rhizobium leguminosarum and other bacteria towards root exudates from legumes and other plants. Microbiology 128, 1179–1188 (1982).
Caetano-Anollés, G., Wrobel-Boerner, E. & Bauer, W. D. Growth and movement of spot inoculated Rhizobium meliloti on the root surface of Alfalfa. Plant Physiol. 98, 1181–1189 (1992).
Massalha, H., Korenblum, E., Malitsky, S., Shapiro, O. H. & Aharoni, A. Live imaging of root–bacteria interactions in a microfluidics setup. Proc. Natl Acad. Sci. USA 114, 4549–4554 (2017). This is a recent study imaging root–bacterial interactions at previously unattainable spatiotemporal resolutions.
Rudrappa, T., Czymmek, K. J., Paré, P. W. & Bais, H. P. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol. 148, 1547–1556 (2008).
Wood, D. C. & Hayasaka, S. S. Chemotaxis of rhizoplane bacteria to amino acids comprising eelgrass (Zostera marina L.) root exudate. J. Exp. Marine Biol. Ecol. 50, 153–161 (1981).
Overmann, J. & Schubert, K. Phototrophic consortia: model systems for symbiotic interrelations between prokaryotes. Arch. Microbiol. 177, 201–208 (2002).
Mark Welch, J. L., Rossetti, B. J., Rieken, C. W., Dewhirst, F. E. & Borisy, G. G. Biogeography of a human oral microbiome at the micron scale. Proc. Natl Acad. Sci. USA 113, E791–E800 (2016).
Castelle, C. J. et al. Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations. Nat. Rev. Microbiol. 16, 629–645 (2018).
Shu, L., Zhang, B., Queller, D. C. & Strassmann, J. E. Burkholderia bacteria use chemotaxis to find social amoeba Dictyostelium discoideum hosts. ISME J. 12, 1977–1993 (2018).
Gast, R. J., Sanders, R. W. & Caron, D. A. Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. Trends Microbiol. 17, 563–569 (2009).
Ohkuma, M. Symbioses of flagellates and prokaryotes in the gut of lower termites. Trends Microbiol. 16, 345–352 (2008).
Dyer, B. D. & Khalsa, O. Surface bacteria of Streblomastix strix are sensory symbionts. Biosystems 31, 169–180 (1993).
Adams, D. G. & Duggan, P. S. Cyanobacteria–bryophyte symbioses. J. Exp. Bot. 59, 1047–1058 (2008).
Lee, J. B. et al. Bacterial cell motility of Burkholderia gut symbiont is required to colonize the insect gut. FEBS Lett. 589, 2784–2790 (2015).
Kikuchi, Y., Hosokawa, T. & Fukatsu, T. An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J. 5, 446 (2010).
Ohbayashi, T. et al. Insect’s intestinal organ for symbiont sorting. Proc. Natl Acad. Sci. USA 112, E5179–E5188 (2015). This study provides a fascinating example of an overlooked mechanism enabling symbiont selection.
Kühn, M. J., Schmidt, F. K., Eckhardt, B. & Thormann, K. M. Bacteria exploit a polymorphic instability of the flagellar filament to escape from traps. Proc. Natl Acad. Sci. USA 114, 6340–6345 (2017).
Davidson, S. K. & Stahl, D. A. Selective recruitment of bacteria during embryogenesis of an earthworm. ISME J. 2, 510 (2008).
Kaufman, M. R., Ikeda, Y., Patton, C., van Dykhuizen, G. & Epel, D. Bacterial symbionts colonize the accessory nidamental gland of the squid Loligo opalescens via horizontal transmission. Biol. Bull. 194, 36–43 (1998).
Barbieri, E. et al. Phylogenetic characterization of epibiotic bacteria in the accessory nidamental gland and egg capsules of the squid Loligo pealei (Cephalopoda: Loliginidae). Environ. Microbiol. 3, 151–167 (2001).
Nilsson, M., Rasmussen, U. & Bergman, B. Cyanobacterial chemotaxis to extracts of host and nonhost plants. FEMS Microbiol. Ecol. 55, 382–390 (2006).
Orphan, V. J., House, C. H., Hinrichs, K.-U., McKeegan, K. D. & DeLong, E. F. Methane-consuming Archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293, 484–487 (2001).
Hentschel, U., Steinert, M. & Hacker, J. Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol. 8, 226–231 (2000).
Chaban, B., Hughes, H. V. & Beeby, M. The flagellum in bacterial pathogens: for motility and a whole lot more. Semin. Cell Dev. Biol. 46, 91–103 (2015).
Butler, S. M. & Camilli, A. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat. Rev. Microbiol. 3, 611 (2005).
Allweiss, B., Dostal, J., Carey, K. E., Edwards, T. F. & Freter, R. The role of chemotaxis in the ecology of bacterial pathogens of mucosal surfaces. Nature 266, 448 (1977).
Bordas, M. A., Balebona, M. C., Rodriguez-Maroto, J. M., Borrego, J. J. & Moriñigo, M. A. Chemotaxis of pathogenic Vibrio strains towards mucus surfaces of gilt-head sea bream (Sparus aurata L.). Appl. Environ. Microbiol. 64, 1573–1575 (1998).
Austin, B. & Austin, D. A. Bacterial Fish Pathogens (Springer, 2012).
Austin, B. & Zhang, X. H. Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett. Appl. Microbiol. 43, 119–124 (2006).
Josenhans, C. & Suerbaum, S. The role of motility as a virulence factor in bacteria. Int. J. Med. Microbiol. 291, 605–614 (2002).
Angus, A. A. et al. Plant-associated symbiotic Burkholderia species lack hallmark strategies required in mammalian pathogenesis. PLOS ONE 9, e83779 (2014).
Krause, A. et al. Complete genome of the mutualistic, N2-fixing grass endophyte Azoarcus sp. strain BH72. Nat. Biotechnol. 24, 1384 (2006).
Bertalan, M. et al. Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5. BMC Genomics 10, 450 (2009).
Kaneko, T. et al. Complete genomic structure of the cultivated rice endophyte Azospirillum sp. B510. DNA Res. 17, 37–50 (2010).
Fouts, D. E. et al. Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in mice. PLOS Genet. 4, e1000141 (2008).
Mitter, B. et al. Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front. Plant Sci. 4, 120 (2013).
Yan, Y. et al. Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc. Natl Acad. Sci. USA 105, 7564–7569 (2008).
Taghavi, S. et al. Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLOS Genet. 6, e1000943 (2010).
Sourjik, V. et al. Mapping of 41 chemotaxis, flagellar and motility genes to a single region of the Sinorhizobium meliloti chromosome. Gene 223, 283–290 (1998).
Crossman, L. C. et al. A common genomic framework for a diverse assembly of plasmids in the symbiotic nitrogen fixing bacteria. PLOS ONE 3, e2567 (2008).
Han, J.-I. et al. Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J. Bacteriol. 193, 1183–1190 (2011).
Gärdes, A. et al. Complete genome sequence of Marinobacter adhaerens type strain (HP15), a diatom-interacting marine microorganism. Stand. Genomic Sci. 3, 97–107 (2010).
Moran, M. A. et al. Ecological genomics of marine roseobacters. Appl. Environ. Microbiol. 73, 4559–4569 (2007).
Hendry, T. A., de Wet, J. R., Dougan, K. E. & Dunlap, P. V. Genome evolution in the obligate but environmentally active luminous symbionts of flashlight Fish. Genome Biol. Evol. 8, 2203–2213 (2016).
Ruby, E. G. et al. Complete genome sequence of Vibrio fischeri: a symbiotic bacterium with pathogenic congeners. Proc. Natl Acad. Sci. USA 102, 3004–3009 (2005).
Stephens, W. Z. et al. Identification of population bottlenecks and colonization factors during assembly of bacterial communities within the Zebrafish intestine. mBio 6, e01163–15 (2015).
McCuaig, B., Pena-Castillo, L. & Dufour, S. C. Metagenomic analysis suggests broad metabolic potential in extracellular symbionts of the bivalve Thyasira cf. gouldi. Preprint at bioRxiv https://www.biorxiv.org/content/10.1101/330373v1 (2018).
Perez, M. & Juniper, S. K. Insights into symbiont population structure among three vestimentiferan tubeworm host species at eastern pacific spreading centers. Appl. Environ. Microbiol. 82, 5197–5205 (2016).
Goffredi, S. K. et al. Genomic versatility and functional variation between two dominant heterotrophic symbionts of deep-sea Osedax worms. ISME J. 8, 908 (2013).
Nakagawa, S. et al. Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont. ISME J. 8, 40 (2013).
Neave, M. J., Michell, C. T., Apprill, A. & Voolstra, C. R. Endozoicomonas genomes reveal functional adaptation and plasticity in bacterial strains symbiotically associated with diverse marine hosts. Sci. Rep. 7, 40579 (2017).
Woyke, T. et al. Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443, 950 (2006).
Nunoura, T. et al. Physiological and genomic features of a novel sulfur-oxidizing gammaproteobacterium belonging to a previously uncultivated symbiotic lineage isolated from a hydrothermal vent. PLOS ONE 9, e104959 (2014).
Dmytrenko, O. et al. The genome of the intracellular bacterium of the coastal bivalve. Solemya velum: a blueprint for thriving in and out of symbiosis. BMC Genomics 15, 924 (2014).
Shibata, T. F. et al. Complete genome sequence of Burkholderia sp. strain RPE64, bacterial symbiont of the bean bug Riptortus pedestris. Genome Announc. 1, e00441–13 (2013).
Takeshita, K. et al. Whole-genome sequence of Burkholderia sp. strain RPE67, a bacterial gut symbiont of the Bean Bug Riptortus pedestris. Genome Announc. 2, e00556–14 (2014).
Ueda, K. et al. Genome sequence of Symbiobacterium thermophilum, an uncultivable bacterium that depends on microbial commensalism. Nucleic Acids Res. 32, 4937–4944 (2004).
Warshan, D. et al. Genomic changes associated with the evolutionary transitions of Nostoc to a plant symbiont. Mol. Biol. Evol. 35, 1160–1175 (2018).
Patterson, A. M. et al. Human gut symbiont Roseburia hominis promotes and regulates innate immunity. Front. Immunol. 8, 1166 (2017).
This research was funded in part by the Gordon and Betty Moore Foundation Marine Microbiology Initiative, through grant GBMF3801 to J.R.S. and R.S. and an Investigator Award (GBMF3783) to R.S., as well as through an Australian Research Council grant (DP180100838) to J.R.S. and J.-B.R., an Australian Research Council Fellowship (DE160100636) to J.-B.R. and a grant from the Simons Foundation (542395) to R.S. as part of the Principles of Microbial Ecosystems (PriME) Collaborative.
V.F., B.L. and J.-B.R. researched data for the article. V.F. carried out the theoretical component of this work. All authors contributed substantially to discussion of the content, wrote the article and reviewed and edited the manuscript before submission.
Nature Reviews Microbiology thanks Y. Kikuchi, M. Mandel and the other anonymous reviewer(s) for their contribution to the peer review of this work.
The authors declare no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The ability of microorganisms to sense chemical gradients and direct their movement either up the gradient towards the source (attraction) or down the gradient away from the source (repulsion).
Filamentous extracellular appendages that are responsible for the active movement of cells in a liquid environment. Beyond cell motility, flagella are also involved in a range of processes including adhesion, secretion of compounds, virulence and differentiation into biofilms.
- Brownian motion
Continuous movement of micrometre-scale particles and organisms in liquid driven by random collisions with water molecules.
The zone immediately surrounding the roots of a plant that is enriched in molecules secreted from the root into the soil, providing a key interface for the ecological relationships and chemical exchanges between plants and soil microorganisms.
The spread of dissolved compounds from an area of high concentration to an area of lower concentration, driven by random fluctuations. This rate is set by the diffusivity (D) of the compound, and the spread of a diffusing cloud progressively slows down as it grows in size.
- Viscous boundary layer
The region of fluid in the immediate vicinity of a surface where the effects of viscosity are substantial. Fluid flow decreases with proximity to the surface.
- Diffusion boundary layer
A region of fluid near a surface where transport of dissolved compounds is dominated by diffusion rather than advection by flow. The size of this region depends on the diffusivity of the compounds and the viscous boundary layer.
A common type of stochastic, chaotic flow composed of interacting vortices across a range of scales.
- Shear flows
A type of flow in which the fluid moves in parallel directions but with changing magnitude. Shear flow exists in regions with gradients in velocity, such as the region between a surface with no flow and a constant external flow parallel to the surface.
- Feeding currents
Fluid motion generated by an organism to increase prey encounter. These currents can be generated through beating cilia (in protists), mouth appendages (in copepods) or specialized ciliated cells (in sponges).
Thin filamentous appendages made out of extracellular protein fibres that are involved in various microbial behaviours, including attachment, twitching motility and virulence.
Viscous aqueous secretion typically produced by specialized cells that has a role in the protection against infectious agents. Mucus coats the gastrointestinal, respiratory and urogenital tracts of most animals, as well as the external surfaces of marine organisms.
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Raina, JB., Fernandez, V., Lambert, B. et al. The role of microbial motility and chemotaxis in symbiosis. Nat Rev Microbiol 17, 284–294 (2019). https://doi.org/10.1038/s41579-019-0182-9
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