Yeasts affect tolerance of Drosophila melanogaster to food substrate with high NaCl concentration

Autoři: A. S. Dmitrieva aff001;  S. B. Ivnitsky aff001;  I. A. Maksimova aff002;  P. L. Panchenko aff001;  A. V. Kachalkin aff002;  A. V. Markov aff001
Působiště autorů: Department of Biological Evolution, Faculty of Biology, Lomonosov Moscow State University, Moscow, Russia aff001;  Department of Soil Biology, Faculty of Soil Science, Lomonosov Moscow State University, Moscow, Russia aff002;  G.K. Skryabin Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, Pushchino, Russia aff003;  Borissiak Paleontological Institute, Russian Academy of Sciences, Moscow, Russia aff004
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224811


The ability of model animal species, such as Drosophila melanogaster, to adapt quickly to various adverse conditions has been shown in many experimental evolution studies. It is usually assumed by default that such adaptation is due to changes in the gene pool of the studied population of macroorganisms. At the same time, it is known that microbiome can influence biological processes in macroorganisms. In order to assess the possible impact of microbiome on adaptation, we performed an evolutionary experiment in which some D. melanogaster lines were reared on a food substrate with high NaCl concentration while the others were reared on the standard (favourable) substrate. We evaluated the reproductive efficiency of experimental lines on the high salt substrate three years after the experiment started. Our tests confirmed that the lines reared on the salty substrate became more tolerant to high NaCl concentration. Moreover, we found that pre-inoculation of the high salt medium with homogenized salt-tolerant flies tended to improve reproductive efficiency of naïve flies on this medium (compared to pre-inoculation with homogenized control flies). The analysis of yeast microbiome in fly homogenates revealed significant differences in number and species richness of yeasts between salt-tolerant and control lines. We also found that some individual yeast lines extracted from the salt-tolerant flies improved reproductive efficiency of naïve flies on salty substrate (compared to baker’s yeast and no yeast controls), whereas the effect of the yeast lines extracted from the control flies tended to be smaller. The yeast Starmerella bacillaris extracted from the salt-tolerant flies showed the strongest positive effect. This yeast is abundant in all salt-tolerant lines, and very rare or absent in all control lines. The results are consistent with the hypothesis that some components of the yeast microbiome of D. melanogaster contribute to to flies’ tolerance to food substrate with high NaCl concentration.

Klíčová slova:

Drosophila melanogaster – Evolutionary adaptation – Food – Larvae – Microbial evolution – Microbiome – Yeast – Fungal evolution


1. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC. Experimental evolution. Trends Ecol Evol. 2012;27(10):547–560. doi: 10.1016/j.tree.2012.06.001 22819306

2. McFall-Ngai MJ. Unseen forces: the influence of bacteria on animal development. Dev Biol. 2002;242:1–14. doi: 10.1006/dbio.2001.0522 11795936

3. Zilber-Rosenberg I, Rosenberg E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev. 2008;32:723–735. doi: 10.1111/j.1574-6976.2008.00123.x 18549407

4. Margulis L, Fester R. Symbiosis as a Source of evolutionary innovation: speciation and morphogenesis. Boston: MIT Press; 1991.

5. 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):355–362. doi: 10.1038/nrmicro1635 17384666

6. Rosenberg E, Sharon G, Zilber-Rosenberg I. The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environ Microbiol. 2009;11(12):2959–2962. doi: 10.1111/j.1462-2920.2009.01995.x 19573132

7. Bordenstein SR, Theis KR. Host biology in light of the microbiota: ten principles of holobionts and hologenomes. PLoS Biol. 2015;13(8):e1002226. doi: 10.1371/journal.pbio.1002226 26284777

8. Erkosar B, Leulier F. Transient adult microbiota, gut homeostasis and longevity: novel insights from the Drosophila model. FEBS Lett. 2014;588(22):4250–4257. doi: 10.1016/j.febslet.2014.06.041 24983497

9. Newell PD, Chaston JM, Wang Y, Winans NJ, Sannino DR, Wong AC-N, Dobson AJ, Kagle J, Douglas AE. In vivo function and comparative genomic analyses of the Drosophila gut microbiota identify candidate symbiosis factors. Front Microbiol. 2014 Nov;4(5):576. doi: 10.3389/fmicb.2014.00576 25408687

10. Hoang D, Kopp A, Chandler JA. Interactions between Drosophila and its natural yeast symbionts—Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship? PeerJ. 2015;3:e1116. doi: 10.7717/peerj.1116 26336636

11. Shaposhnikov GK. The specifity and emergence of adaptations to the new hosts in aphids (Homoptera, Aphidoidea) in the process of natural selection (experimental studies). Entomologicheskoye Obozreniye. 1961;40(4):739–762 (in Russian).

12. Munson MA, Baumann P, Kinsey MG. Buchnera gen. nov. and Buchnera aphidicola sp. nov., a Taxon Consisting of the Mycetocyte-Associated, Primary Endosymbionts of Aphids. Int J Syst Bacteriol. 1991;41(4): 566–568.

13. Akman Gündüz E, Douglas AE. Symbiotic bacteria enable insect to use a nutritionally inadequate diet. P Roy Soc Ser B-Biol. 2009;276:987–991.

14. Dunbar HE, Wilson ACC, Ferguson NR, Moran NA. Aphid thermal tolerance is governed by a point mutation in bacterial symbionts. PLoS Biol. 2007;5(5):e96. doi: 10.1371/journal.pbio.0050096 17425405

15. Dodd DMB. Reproductive isolation as a consequence of adaptive divergence in Drosophila pseudoobscura. Evolution. 1989;43:1308–1311. doi: 10.1111/j.1558-5646.1989.tb02577.x 28564510

16. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc Natl Acad Sci USA. 2010;107:20051–20056. doi: 10.1073/pnas.1009906107 21041648

17. Najarro MA, Sumethasorn M, Lamoureux A, Turner TL. Choosing mates based on the diet of your ancestors: replication of non-genetic assortative mating in Drosophila melanogaster. PeerJ. 2015;3:e1173. doi: 10.7717/peerj.1173 26339551

18. Leftwich PT, Clarke NVE, Hutchings MI, Chapman T. 2017. Gut microbiomes and reproductive isolation in Drosophila. Proc Natl Acad Sci USA. 2017;114(48):12767–12772. doi: 10.1073/pnas.1708345114 29109277

19. Belkina EG, Naimark EB, Gorshkova AA, Markov AV. Does adaptation to different diets result in assortative mating? Ambiguous results from experiments on Drosophila. J Evolution Biol. 2018;31:1803–1814.

20. Te Velde JH, Molthoff CFM, Scharloo W. The function of anal papillae in salt adaptation of Drosophila melanogaster larvae. J Evolution Biol. 1988;2:139–153.

21. Stergiopoulos K, Cabrero P, Davies SA, Dow JA. Salty dog, an SLC5 symporter, modulates Drosophila response to salt stress. Physiol Genomics. 2009;37:1–11. doi: 10.1152/physiolgenomics.90360.2008 19018044

22. Waddington CH. Canalization of development and genetic assimilation of acquired characters. Nature. 1959;183:1654–1655. doi: 10.1038/1831654a0 13666847

23. Long TAF, Rowe L, Agrawal AF. The effects of selective history and environmental heterogeneity on inbreeding depression in experimental populations of Drosophila melanogaster. Am Nat. 2013;181:532–544. doi: 10.1086/669675 23535617

24. Arbuthnott D, Rundle HD. Misalignment of natural and sexual selection among divergently adapted Drosophila melanogaster populations. Anim Behav. 2014;87:45–51.

25. Markov AV, Ivnitsky SB, Kornilova MB, Naimark EB, Shirokova NG, Perfilieva KS. Maternal effect masks the adaptation to adverse conditions and hampers divergence in Drosophila melanogaster. Zh Obshch Biol. 2015;76(6):429–437 (in Russian). doi: 10.1134/s2079086416050054 26852569

26. Dmitrieva АS, Ivnitsky SB, Markov AV. Adaptation of Drosophila melanogaster to Unable Feed Substrate Is Accompanied by Expansion of Trophic Niche. Zh Obshch Biol. 2017;7(5):369–379(in Russian).

27. Gorshkova AA, Fetisova ES, Yakovleva EY, Naimark EB, Markov AV. Influence of the heterogeneity of the spatial structure on Drosophila melanogaster adaptation to adverse food substrates: the results of the evolutionary experiments. Zh Obshch Biol. 2018;79(1):3–17 (in Russian).

28. Herbst DB. Gradients of salinity stress, environmental stability and water chemistry as a templet for defining habitat types and physiological strategies in inland salt waters. Hydrobiologia. 2001;466:209–219.

29. Brummel T, Ching A, Seroude L, Simon AF, Benzer S. Drosophila lifespan enhancement by exogenous bacteria. Proc Natl Acad Sci USA. 2004;101:12974–12979. doi: 10.1073/pnas.0405207101 15322271

30. Shin SC, Kim SH, You H, Kim B, Kim AC, Lee KA, Yoon JH, Ryu JH, Lee WJ. Drosophila microbiota modulates host developmental and metabolic homeostasis via insulin signaling. Science. 2011;334:670–674. doi: 10.1126/science.1212782 22053049

31. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab. 2011;14:403–414. doi: 10.1016/j.cmet.2011.07.012 21907145

32. Blum JE, Fischer CN, Miles J, Handelsman J. Frequent replenishment sustains the beneficial microbiota of Drosophila melanogaster. MBio. 2013;4:e00860. doi: 10.1128/mBio.00860-13 24194543

33. Erkosar B, Storelli G, Defaye A, Leulier F. Host-intestinal microbiota mutualism: ‘‘learning on the fly”. Cell Host Microbe. 2013;13:8–14. doi: 10.1016/j.chom.2012.12.004 23332152

34. Combe BE, Defaye A, Bozonnet N, Puthier D, Royet J, Leulier F (2014) Drosophila Microbiota Modulates Host Metabolic Gene Expression via IMD/NF-κB Signaling. PLoS ONE;9(4):e94729. doi: 10.1371/journal.pone.0094729 24733183

35. Wong AC-N, Dobson AJ, Douglas AE. Gut microbiota dictates the metabolic response of Drosophila to diet. J Exp Biol. 2014;217:1894–1901. doi: 10.1242/jeb.101725 24577449

36. Wong AC-N, Vanhove AS, Watnick PI. The interplay between intestinal bacteria and host metabolism in health and disease: lessons from Drosophila melanogaster. Dis Model Mech. 2016;9:271–281. doi: 10.1242/dmm.023408 26935105

37. Chaston JM, Dobson AJ, Newell PD, Douglas AE. Host Genetic Control of the Microbiota Mediates the Drosophila Nutritional Phenotype. Appl Environ Microbiol. 2015;82(2):671–679. doi: 10.1128/AEM.03301-15 26567306

38. Yamada R, Deshpande SA, Bruce KD, Mak EM, Ja WW. Microbes promote amino acid harvest to rescue undernutrition in Drosophila. Cell Rep. 2015;10:865–872. doi: 10.1016/j.celrep.2015.01.018 25683709

39. Chandler JA, Eisen JA, Kopp A. Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts. Appl Envir Microbiol. 2012;78(20):7327–7336.

40. Starmer WT. A comparison of Drosophila habitats according to the physiological attributes of the associated yeast communities. Evolution. 1981;35(1):38–52. doi: 10.1111/j.1558-5646.1981.tb04856.x 28563455

41. Starmer WT, Barker JSF, Phaff HJ, Fogleman JC. Adaptations of Drosophila and Yeasts: their Interactions with the Volatile 2-propanol in the Cactus–Microorganism–Drosophila Model System. Aust J Biol Sci. 1986;39:69–77. 3778359

42. Anagnostou C, Dorsch M, Rohlfs M. Influence of dietary yeasts on Drosophila melanogaster life-history traits. Entomol Exp Appl. 2010;136:1–11.

43. Panchenko PL, Kornilova MB, Perfilieva KS, Markov AV. Contribution of Symbiotic Microbiota to Adaptation of Drosophila melanogaster to an Unfavourable Growth Medium. Biol Bull+. 2017;44(4):345–354 (in Russian).

44. Ivnitsky SB, Maksimova IA, Panchenko PL, Dmitrieva АS, Kornilova MB, Perfilieva KS, Markov AV. A role of microbiota in adaptation of Drosophila melanogaster to food substrate with high NaCl concentration. Zh Obshch Biol. 2018;79(5):393–403 (in Russian).

45. Glushakova АМ, Kachalkin АV, Chernov IY. Specific features of the dynamics of epiphytic and soil yeast communities in the thickets of Indian balsam on mucky gley soil. Eurasian Soil Sci+. 2011;44(8):886–892.

46. Broderick NA, Lemaitre B. Gut-associated microbes of Drosophila melanogaster. Gut Microbes. 2012 Jul-Aug;3(4):307–321. doi: 10.4161/gmic.19896 22572876

47. Wong AC-N, Chaston JM, Douglas AE. The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis. ISME J. 2013;7:1922–1932. doi: 10.1038/ismej.2013.86 23719154

48. Stamps JA, Yang LH, Morales VM, Boundy-Mills KL. Drosophila regulate yeast density and increase yeast community similarity in a natural substrate. PLoS One. 2012;7(7):e42238. doi: 10.1371/journal.pone.0042238 22860093

49. Reuter M, Bell G, Greig D. Increased outbreeding in yeast in response to dispersal by an insect vector. Curr Biol. 2007 Feb 6;17(3):R81–3. doi: 10.1016/j.cub.2006.11.059 17276903

50. Coluccio AE, Rodriguez RK, Kernan MJ, Neiman AM. The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila. PLoS One. 2008;3(8):e2873. doi: 10.1371/journal.pone.0002873 18682732

51. Sipiczki M. Candida zemplinina sp. nov., an osmotolerant and psychrotolerant yeast that ferments sweet botrytized wines. Int J Syst Evol Microbiol. 2003;53:2079–2083. doi: 10.1099/ijs.0.02649-0 14657149

52. Csoma H, Ács-Szabó L, Papp LA, Sipiczki M. Application of different markers and data-analysis tools to the examination of biodiversity can lead to different results: a case study with Starmerella bacillaris (synonym Candida zemplinina) strains. FEMS Yeast Res. 2018 Aug 1;18(5). doi: 10.1093/femsyr/foy021 29518226

53. Phaff HJ, Miller MW, Shifrine M. The taxonomy of yeasts isolated from Drosophila in the Yosemite region of California. Antonie van Leeuwenhoek. 1956;22:145–61. doi: 10.1007/bf02538322 13340701

54. Mueller UG, Rehner SA, Schultz TR. The Evolution of Agriculture in Ants. Science. 1998;281(5385):2034–2038. doi: 10.1126/science.281.5385.2034 9748164

55. Aanen DK, Eggleton P, Rouland-Lefèvre C, Guldberg-Frøslev T, Rosendahl S, Boomsma JJ. The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci USA. 2002;99(23):14887–14892. doi: 10.1073/pnas.222313099 12386341

56. Phaff HJ, Knapp EP. The taxonomy of yeasts found in exudates of certain trees and other natural breeding sites of some species of Drosophila. Antonie Van Leeuwenhoek. 1956; 22(2):117–130. doi: 10.1007/bf02538319 13340698

57. Ha EM, Lee KA, Park SH, Kim SH, Nam HJ, Lee HY, Kang D, Lee WJ. Regulation of DUOX by the Gαq-Phospholipase Cβ-Ca2+ pathway in Drosophila gut immunity. Dev Cell. 2009 Mar;16(3):386–397. doi: 10.1016/j.devcel.2008.12.015 19289084

Článek vyšel v časopise


2019 Číslo 11