Darwinian selection of host and bacteria supports emergence of Lamarckian-like adaptation of the system as a whole
Tóm tắt
The relatively fast selection of symbiotic bacteria within hosts and the potential transmission of these bacteria across generations of hosts raise the question of whether interactions between host and bacteria support emergent adaptive capabilities beyond those of germ-free hosts. To investigate possibilities for emergent adaptations that may distinguish composite host-microbiome systems from germ-free hosts, we introduce a population genetics model of a host-microbiome system with vertical transmission of bacteria. The host and its bacteria are jointly exposed to a toxic agent, creating a toxic stress that can be alleviated by selection of resistant individuals and by secretion of a detoxification agent (“detox”). We show that toxic exposure in one generation of hosts leads to selection of resistant bacteria, which in turn, increases the toxic tolerance of the host’s offspring. Prolonged exposure to toxin over many host generations promotes anadditional form of emergent adaptation due to selection of hosts based on detox produced by their bacterial community as a whole (as opposed to properties of individual bacteria). These findings show that interactions between pure Darwinian selections of host and its bacteria can give rise to emergent adaptive capabilities, including Lamarckian-like adaptation of the host-microbiome system. This article was reviewed by Eugene Koonin, Yuri Wolf and Philippe Huneman.
Tài liệu tham khảo
Koonin EV, Wolf YI. Is evolution Darwinian or/and Lamarckian? Biol Direct. 2009;4:42.
Noble D, Jablonka E, Joyner MJ, Muller GB, Omholt SW. Evolution evolves: physiology returns to Centre stage. J Physiol. 2014;592:2237–44.
Rosenberg E, Sharon G, Zilber-Rosenberg I. The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environ Microbiol. 2009;11:2959–62.
Laland K, Uller T, Feldman M, Sterelny K, Muller BG, Moczek A, Jablonka E, Odling-Smee J, Wray GA, Hoekstra HE, et al. Does evolutionary theory need a rethink? In: Nature; 2014.
Soen Y. Environmental disruption of host-microbe co-adaptation as a potential driving force in evolution. Front Genet. 2014;5.
Soen Y, Knafo M, Elgart M. A principle of organization which facilitates broad Lamarckian-like adaptations by improvisation. Biol Direct. 2015;10(1):1–17.
Braun E. The unforeseen challenge: from genotype-to-phenotype in cell populations. Rep Prog Phys. 2015;78:036602.
Seong K-H, Li D, Shimizu H, Nakamura R, Ishii S. Inheritance of stress-induced, ATF-2-dependent epigenetic change. Cell. 2011;145(7):1049–61.
Stern S, Fridmann-Sirkis Y, Braun E, Soen Y. Epigenetically heritable alteration of fly development in response to toxic challenge. Cell Rep. 2012;1.
Rechavi O, Minevich G, Hobert O. Transgenerational inheritance of an acquired small RNA-based antiviral response in C. elegans. Cell. 2011:147, 1248–1156.
Jablonka E, Raz G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol. 2009;84.
Koonin EV. Viruses and mobile elements as drivers of evolutionary transitions. Philos Trans R Soc Lond B Biol Sci. 2016;371(1701):20150442.
Koonin EV, Wolf YI. Just how Lamarckian is CRISPR-Cas immunity: the continuum of evolvability mechanisms. Biol Direct. 2016;11(1):9.
Odling-Smee J. Niche inheritance: a possible basis for classifying multiple inheritance Systems in Evolution. Biological Theory. 2007;2:276–89.
Zilber-Rosenberg I, Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev. 2008;32.
Gilbert SF, Sapp J, Tauber AI. A symbiotic view of life: we have never been individuals. Q Rev Biol. 2012;87.
Margulis L, editor. Symbiosis as a source of evolutionary innovation: speciation and morphogenesis. Cambridge: MIT press; 1991.
Dittmer J, van Opstal EJ, Shropshire JD, Bordenstein SR, Hurst GD, Brucker RM: Disentangling a Holobiont - recent advances and perspectives in Nasonia wasps. Front Microbiol 2016, 7:1478.
Frydman HM, Li JM, Robson DN, Wieschaus E. Somatic stem cell niche tropism in Wolbachia. Nature. 2006;441(7092):509–12.
Brooks AW, Kohl KD, Brucker RM, van Opstal EJ, Bordenstein SR. Phylosymbiosis: relationships and functional effects of microbial communities across host evolutionary history. PLoS Biol. 2016;14(11):e2000225.
Remigi P, Capela D, Clerissi C, Tasse L, Torchet R, Bouchez O, Batut J, Cruveiller S, Rocha EP, Masson-Boivin C. Transient hypermutagenesis accelerates the evolution of legume endosymbionts following horizontal gene transfer. PLoS Biol. 2014;12(9):e1001942.
Damore JA, Gore J. A slowly evolving host moves first in symbiotic interactions. Evolution. 2011;65(8):2391–98.
Kopac SM, Klassen JL. Can they make it on their own? Hosts, microbes, and the Holobiont niche. Front Microbiol. 2016;7.
Bruno JF, Stachowicz JJ, Bertness MD. Inclusion of facilitation into ecological theory. Trends Ecol Evol. 2003;18(3):119–25.
Lewin-Epstein O, Aharonov R, Hadany L. Microbes can help explain the evolution of host altruism. Nat Commun. 2017;8:14040.
Bordenstein SR, Theis KR. Host biology in light of the microbiome: ten principles of Holobionts and Hologenomes. PLoS Biol. 2015;13(8):e1002226.
Macke E, Tasiemski A, Massol F, Callens M, Decaestecker E. Life history and eco-evolutionary dynamics in light of the gut microbiota. Oikos. 2017;126(4):508–31.
Vavre F, Kremer N. Microbial impacts on insect evolutionary diversification: from patterns to mechanisms. Curr Opin Insect Sci. 2014;4:29–34.
McFall-Ngai M, Hadfield MG, Bosch TC, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, et al. Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A. 2013;110(9):3229–36.
McFall-Ngai MJ. Unseen forces: the influence of bacteria on animal development. Dev Biol. 2002;242(1):1–14.
Peiffer JA, Spor A, Koren O, Jin Z, Tringe SG, Dangl JL, Buckler ES, Ley RE. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proc Natl Acad Sci U S A. 2013;110(16):6548–53.
Goodrich JK, Davenport ER, Beaumont M, Jackson MA, Knight R, Ober C, Spector TD, Bell JT, Clark AG, Ley RE. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe. 2016;19(5):731–43.
Remigi P, Zhu J, Young JPW, Masson-Boivin C. Symbiosis within Symbiosis: evolving nitrogen-fixing legume Symbionts. Trends Microbiol. 2016;24(1):63–75.
Beaumont M, Goodrich JK, Jackson MA, Yet I, Davenport ER, Vieira-Silva S, Debelius J, Pallister T, Mangino M, Raes J, et al. Heritable components of the human fecal microbiome are associated with visceral fat. Genome Biol. 2016;17(1):189.
Fridmann-Sirkis Y, Stern S, Elgart M, Galili M, Zeisel A, Shental N, Soen Y. Delayed development induced by toxicity to the host can be inherited by a bacterial-dependent, transgenerational effect. Front Genet. 2014;5:27.
Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I. The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol. 2007;5(5):355–62.
Douglas AE, Werren JH. Holes in the Hologenome: why host-microbe symbioses are not Holobionts. MBio. 2016;7(2):e02099.
Moran NA, Sloan DB. The Hologenome concept: helpful or hollow? PLoS Biol. 2015;13(12):e1002311.
Theis KR, Dheilly NM, Klassen JL, Brucker RM, Baines JF, Bosch TC, Cryan JF, Gilbert SF, Goodnight CJ, Lloyd EA, et al. Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes. mSystems. 2016;1(2).
Roughgarden J, Gilbert SF, Rosenberg E, Zilber-Rosenberg I, Lloyd EA. Holobionts as units of selection and a model of their population dynamics and evolution. Biological Theory. 2018;13(1):44–65.
Castillo-Chavez FBC. Mathematical models in population biology and epidemiology. New York: Springer-Verlag; 2000.
Crow JF, Kimura M. An introduction to population genetics theory. New York: Harper & Row; 1970.
Douglas AE. The microbial dimension in insect nutritional ecology. Funct Ecol. 2009;23(1):38–47.
Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiol Rev. 2010;90(3):859–904.
Lee WJ, Brey PT. How microbiomes influence metazoan development: insights from history and Drosophila modeling of gut-microbe interactions. Annu Rev Cell Dev Bi. 2013;29:571–92.
Mouton L, Henri H, Charif D, Bouletreau M, Vavre F. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol Lett. 2007;3(2):210–3.
Muscatine L, Pool RR. Regulation of numbers of intracellular algae. Proc R Soc Lond B Biol Sci. 1979;204(1155):131–9.
Fishman Y, Zlotkin E, Sher D. Expulsion of symbiotic algae during feeding by the green hydra--a mechanism for regulating symbiont density? PLoS One. 2008;3(7):e2603.
Siciliano SD, Fortin N, Mihoc A, Wisse G, Labelle S, Beaumier D, Ouellette D, Roy R, Whyte LG, Banks MK, et al. Selection of specific endophytic bacterial genotypes by plants in response to soil contamination. Appl Environ Microbiol. 2001;67(6):2469–75.
Ceja-Navarro JA, Vega FE, Karaoz U, Hao Z, Jenkins S, Lim HC, Kosina P, Infante F, Northen TR, Brodie EL. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat Commun. 2015;6:7618.
Tetard-Jones C, Edwards R. Potential roles for microbial endophytes in herbicide tolerance in plants. Pest Manag Sci. 2016;72(2):203–9.
Waddington CH. Genetic assimilation of the bithorax phenotype. Evolution. 1956;10:1–13.
Gibson G, Hogness DS. Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability. Science. 1996;271(5246):200–3.
Ridley EV, Wong AC, Douglas AE. Microbe-dependent and nonspecific effects of procedures to eliminate the resident microbiota from Drosophila melanogaster. Appl Environ Microbiol. 2013;79(10):3209–14.
Brummel T, Ching A, Seroude L, Simon AF, Benzer S. Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci U S A. 2004;101(35):12974–9.
Berg M, Stenuit B, Wang A, Ho JA, Alvarez-Cohen L, Shapira M: Assembly of the Caenorhabditis elegans gut microbiota from diverse soil microbial environments. ISME J, Accepted 2016.
Elgart M, Stern S, Salton O, Gnainsky Y, Heifetz Y, Soen Y. Impact of gut microbiota on the fly's germ line. Nat Commun. 2016;7:11280.
Stern S, Snir O, Mizrachi E, Galili M, Zaltsman I, Soen Y. Reduction in maternal polycomb levels contributes to transgenerational inheritance of a response to toxic stress in flies. J Physiol. 2014;592(Pt 11):2343–55.
Miller GA, Islam MS, Claridge TD, Dodgson T, Simpson SJ. Swarm formation in the desert locust Schistocerca gregaria: isolation and NMR analysis of the primary maternal gregarizing agent. J Exp Biol. 2008;211(Pt 3):370–6.
Werren JH. Biology of Wolbachia. Annu Rev Entomol. 1997;42:587–609.
Bright M, Bulgheresi S. A complex journey: transmission of microbial symbionts. Nat Rev Microbiol. 2010;8(3):218–30.
Brandvain Y, Goodnight C, Wade MJ. Horizontal transmission rapidly erodes disequilibria between organelle and symbiont genomes. Genetics. 2011;189(1):397–404.
Fitzpatrick BM. Symbiote transmission and maintenance of extra-genomic associations. Front Microbiol. 2014;5:46.
Asnicar F, Manara S, Zolfo M, Truong DT, Scholz M, Armanini F, Ferretti P, Gorfer V, Pedrotti A, Tett A, et al. Studying Vertical Microbiome Transmission from Mothers to Infants by Strain-Level Metagenomic Profiling. mSystems. 2017;2(1).
Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R. Bacterial community variation in human body habitats across space and time. Science. 2009;326(5960):1694–7.
Blekhman R, Goodrich JK, Huang K, Sun Q, Bukowski R, Bell JT, Spector TD, Keinan A, Ley RE, Gevers D, et al. Host genetic variation impacts microbiome composition across human body sites. Genome Biol. 2015;16:191.
Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, Beaumont M, Van Treuren W, Knight R, Bell JT, et al. Human genetics shape the gut microbiome. Cell. 2014;159(4):789–99.
Dicksved J, Halfvarson J, Rosenquist M, Jarnerot G, Tysk C, Apajalahti J, Engstrand L, Jansson JK. Molecular analysis of the gut microbiota of identical twins with Crohn's disease. ISME J. 2008;2(7):716–27.
Young VB, Schmidt TM. Antibiotic-associated diarrhea accompanied by large-scale alterations in the composition of the fecal microbiota. J Clin Microbiol. 2004;42(3):1203–6.
Schreier HI, Soen Y, Brenner N. Exploratory adaptation in large random networks. Nat Commun. 2017;8:14826.