Salt concentration in substrate modulates the composition of bacterial and yeast microbiomes of Drosophila melanogaster

Ekaterina Yakovleva , Irina Danilova , Irina Maximova , Alexander Shabaev , Anastasia Dmitrieva , Andrey Belov , Alexandra Klyukina , Ksenia Perfilieva , Elizaveta Bonch-Osmolovskaya , Alexander Markov

Microbiome Research Reports ›› 2024, Vol. 3 ›› Issue (2) : 19

PDF
Microbiome Research Reports ›› 2024, Vol. 3 ›› Issue (2) :19 DOI: 10.20517/mrr.2023.56
Original Article

Salt concentration in substrate modulates the composition of bacterial and yeast microbiomes of Drosophila melanogaster

Author information +
History +
PDF

Abstract

Aim: Microbiomes influence the physiology and behavior of multicellular organisms and contribute to their adaptation to changing environmental conditions. However, yeast and bacterial microbiota have usually been studied separately; therefore, the interaction between bacterial and yeast communities in the gut of Drosophila melanogaster (D. melanogaster) is often overlooked. In this study, we investigate the correlation between bacterial and yeast communities in the gut of D. melanogaster.

Methods: We studied the shifts in the joint microbiome of Drosophila melanogaster, encompassing both yeasts and bacteria, during adaptation to substrate with varying salt concentrations (0%, 2%, 4%, and 7%) using plating for both yeasts and bacteria and NGS-sequencing of variable 16S rRNA gene regions for bacteria.

Results: The microbiome of flies and their substrates was gradually altered at moderate NaCl concentrations (2% and 4% compared with the 0% control) and completely transformed at high salt concentrations (7%). The relative abundance of Acetobacter, potentially beneficial to D. melanogaster, decreased as NaCl concentration increased, whereas the relative abundance of the more halotolerant lactobacilli first increased, peaking at 4% NaCl, and then declined dramatically at 7%. At this salinity level, potentially pathogenic bacteria of the genera Leuconostoc and Providencia were dominant. The yeast microbiome of D. melanogaster also undergoes significant changes with an increase in salt concentration in the substrate. The total yeast abundance undergoes nonlinear changes: it is lowest at 0% salt concentration and highest at 2%-4%. At a 7% concentration, the yeast abundance in flies and their substrate is lower than at 2%-4% but significantly higher than at 0%.

Conclusions: The abundance and diversity of bacteria that are potentially beneficial to the flies decreased, while the proportion of potential pathogens, Leuconostoc and Providencia, increased with an increase in salt concentration in the substrate. In samples with a relatively high abundance and/or diversity of yeasts, the corresponding indicators for bacteria were often lowered, and vice versa. This may be due to the greater halotolerance of yeasts compared to bacteria and may also indicate antagonism between these groups of microorganisms.

Keywords

Fruit fly / holobiont / adaptation / high salinity substrate / Acetobacter / lactobacteria / bacterial and yeast microbiota

Cite this article

Download citation ▾
Ekaterina Yakovleva, Irina Danilova, Irina Maximova, Alexander Shabaev, Anastasia Dmitrieva, Andrey Belov, Alexandra Klyukina, Ksenia Perfilieva, Elizaveta Bonch-Osmolovskaya, Alexander Markov. Salt concentration in substrate modulates the composition of bacterial and yeast microbiomes of Drosophila melanogaster. Microbiome Research Reports, 2024, 3(2): 19 DOI:10.20517/mrr.2023.56

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Erkosar B,Defaye A.Host-intestinal microbiota mutualism: “learning on the fly”.Cell Host Microbe2013;13:8-14

[2]

Erkosar B.Transient adult microbiota, gut homeostasis and longevity: novel insights from the Drosophila model.FEBS Lett2014;588:4250-7

[3]

Newell PD.Interspecies interactions determine the impact of the gut microbiota on nutrient allocation in Drosophila melanogaster.Appl Environ Microbiol2014;80:788-96 PMCID:PMC3911109

[4]

Hoang D,Chandler JA.Interactions between Drosophila and its natural yeast symbionts - Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship?.PeerJ2015;3:e1116 PMCID:PMC4556146

[5]

Wong ACN,Watnick PI.The interplay between intestinal bacteria and host metabolism in health and disease: lessons from Drosophila melanogaster.Dis Model Mech2016;9:271-81 PMCID:PMC4833331

[6]

Trinder M,Dube JS.Drosophila melanogaster as a high-throughput model for host-microbiota interactions.Front Microbiol2017;8:751 PMCID:PMC5408076

[7]

Douglas AE.The Drosophila model for microbiome research.Lab Anim2018;47:157-64 PMCID:PMC6586217

[8]

Te Velde JH, Molthoff CFM, Scharloo W. The function of anal papillae in salt adaptation of Drosophila melanogaster larvae.J Evolution Biol1988;1:139-53

[9]

Stergiopoulos K,Davies SA.Salty dog, an SLC5 symporter, modulates Drosophila response to salt stress.Physiol Genomics2009;37:1-11 PMCID:PMC2661102

[10]

Waddington CH.Canalization of development and genetic assimilation of acquired characters.Nature1959;183:1654-5

[11]

Long TAF,Agrawal AF.The effects of selective history and environmental heterogeneity on inbreeding depression in experimental populations of Drosophila melanogaster.Am Nat2013;181:532-44

[12]

Arbuthnott D.Misalignment of natural and sexual selection among divergently adapted Drosophila melanogaster populations.Animal Behaviour2014;87:45-51

[13]

Broderick NA.Gut-associated microbes of Drosophila melanogaster.Gut Microbes2012;3:307-21 PMCID:PMC3463489

[14]

Zheng J,Salvetti E.A taxonomic note on the genus Lactobacillus: description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae.Int J Syst Evol Microbiol2020;70:2782-858

[15]

Wong ACN,Douglas AE.The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis.ISME J2013;7:1922-32 PMCID:PMC3965314

[16]

Blum JE,Miles J.Frequent replenishment sustains the beneficial microbiome of Drosophila melanogaster.mBio2013;4:e00860-13 PMCID:PMC3892787

[17]

Obadia B,Zhang V.Probabilistic invasion underlies natural gut microbiome stability.Curr Biol2017;27:1999-2006.e8 PMCID:PMC5555957

[18]

Pais IS,Sporniak M.Drosophila melanogaster establishes a species-specific mutualistic interaction with stable gut-colonizing bacteria.PLoS Biol2018;16:e2005710 PMCID:PMC6049943

[19]

Vandehoef C,Karpac J.Dietary adaptation of microbiota in Drosophila requires NF-κB-dependent control of the translational regulator 4E-BP.Cell Rep2020;31:107736 PMCID:PMC7366522

[20]

Charroux B.Gut-microbiota interactions in non-mammals: what can we learn from Drosophila?.Semin Immunol2012;24:17-24

[21]

Shin SC,You H.Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling.Science2011;334:670-4

[22]

Brummel T,Seroude L,Benzer S.Drosophila lifespan enhancement by exogenous bacteria.Proc Natl Acad Sci U S A2004;101:12974-9 PMCID:PMC516503

[23]

Sannino DR,Edwards K,Buchon N.The Drosophila melanogaster gut microbiota provisions thiamine to its host.mBio2018;9:e00155-18 PMCID:PMC5845000

[24]

Schretter CE,Bartos I.A gut microbial factor modulates locomotor behaviour in Drosophila.Nature2018;563:402-6 PMCID:PMC6237646

[25]

Mair W,Partridge L.Calories do not explain extension of life span by dietary restriction in Drosophila.PLoS Biol2005;3:e223 PMCID:PMC1140680

[26]

Lee KP,Clissold FJ.Lifespan and reproduction in Drosophila: new insights from nutritional geometry.Proc Natl Acad Sci U S A2008;105:2498-503 PMCID:PMC2268165

[27]

Anagnostou C,Rohlfs M.Influence of dietary yeasts on Drosophila melanogaster life-history traits.Entomol Exp Appl2010;136:1-11

[28]

Carvalho M,Sampaio JL.Survival strategies of a sterol auxotroph.Development2010;137:3675-85 PMCID:PMC2964098

[29]

Piper MDW,Leitão-Gonçalves R.A holidic medium for Drosophila melanogaster.Nat Methods2014;11:100-5 PMCID:PMC3877687

[30]

Sohal RS.Caloric restriction and the aging process: a critique.Free Radic Biol Med2014;73:366-82 PMCID:PMC4111977

[31]

Wu Q,Cheng X.Sexual dimorphism in the nutritional requirement for adult lifespan in Drosophila melanogaster.Aging Cell2020;19:e13120 PMCID:PMC7059147

[32]

Zanco B,Sgrò CM.A dietary sterol trade-off determines lifespan responses to dietary restriction in Drosophila melanogaster females.Elife2021;10:e62335 PMCID:PMC7837700

[33]

Henry Y,Colinet H.Dietary nutrient balance shapes phenotypic traits of Drosophila melanogaster in interaction with gut microbiota.Comp Biochem Physiol A Mol Integr Physiol2020;241:110626

[34]

Klepsatel P,Gáliková M.Temperature induces changes in Drosophila energy stores.Sci Rep2019;9:5239 PMCID:PMC6437209

[35]

Osborne AJ.A ‘phenotypic hangover’: the predictive adaptive response and multigenerational effects of altered nutrition on the transcriptome of Drosophila melanogaster.Environ Epigenet2017;3:dvx019 PMCID:PMC5804559

[36]

Duxbury EML.Sex-specific responses of life span and fitness to variation in developmental versus adult diets in Drosophila melanogaster.J Gerontol A Biol Sci Med Sci2020;75:1431-8 PMCID:PMC7357588

[37]

Stamps JA,Morales VM.Drosophila regulate yeast density and increase yeast community similarity in a natural substrate.PLoS One2012;7:e42238 PMCID:PMC3409142

[38]

Becher PG,Rozpędowska E.Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development.Funct Ecol2012;26:822-8

[39]

Reuter M,Greig D.Increased outbreeding in yeast in response to dispersal by an insect vector.Curr Biol2007;17:R81-3

[40]

Coluccio AE,Kernan MJ.The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila.PLoS One2008;3:e2873 PMCID:PMC2478712

[41]

Ivnitsky SB,Panchenko PL.Microbiome affects the adaptation of Drosophila melanogaster to a high NaCl concentration.Biol Bull Rev2019;9:465-74

[42]

Dmitrieva AS,Maksimova IA,Kachalkin AV.Yeasts affect tolerance of Drosophila melanogaster to food substrate with high NaCl concentration.PLoS One2019;14:e0224811 PMCID:PMC6834263

[43]

Dmitrieva AS,Kachalkin AV.Age-related changes in the yeast component of the Drosophila melanogaster microbiome.Microbiology2021;90:229-36

[44]

Dmitrieva AS,Maksimova IA,Markov AV.Changes in the symbiotic yeast of Drosophila melanogaster during adaptation to substrates with an increased NaCl content.Biol Bull Rev2023;13:1-8

[45]

Panchenko PL,Perfilieva KS.Contribution of symbiotic microbiota to adaptation of Drosophila melanogaster to an unfavorable growth medium.Biol Bull Russ Acad Sci2017;44:345-54

[46]

Dmitrieva AS,Markov AV.Adaptation of Drosophila melanogaster to unfavorable feed substrate is accompanied by expansion of trophic niche.Biol Bull Rev2017;7:369-79

[47]

Belkina EG,Gorshkova AA.Does adaptation to different diets result in assortative mating? Ambiguous results from experiments on Drosophila.J Evol Biol2018;31:1803-14

[48]

Marchesi JR,Weightman AJ.Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rRNA.Appl Environ Microbiol1998;64:795-9 PMCID:PMC106123

[49]

Weisburg WG,Pelletier DA.16S ribosomal DNA amplification for phylogenetic study.J Bacteriol1991;173:697-703 PMCID:PMC207061

[50]

DeLong EF.Archaea in coastal marine environments.Proc Natl Acad Sci U S A1992;89:5685-9 PMCID:PMC49357

[51]

Lane DJ. 16S/23S rRNA sequencing. In: Nucleic acid techniques in bacterial systematic. New York: Wiley; 1991. pp. 115-75. Available from: https://search.worldcat.org/title/nucleic-acid-techniques-in-bacterial-systematics/oclc/22310197. [Last accessed on 27 Feb 2024]

[52]

Hugerth LW,Lundin S.DegePrime, a program for degenerate primer design for broad-taxonomic-range PCR in microbial ecology studies.Appl Environ Microbiol2014;80:5116-23 PMCID:PMC4135748

[53]

Merkel AY,Podosokorskaya OA.Analysis of 16S rRNA primer systems for profiling of thermophilic microbial communities.Microbiology2019;88:671-80

[54]

Vortsepneva E,Klyukina A.Microbial associations of shallow-water Mediterranean marine cave Solenogastres (Mollusca).PeerJ2021;9:e12655 PMCID:PMC8684320

[55]

Gavrilov SN,Kublanov IV.Microbial communities of polymetallic deposits’ acidic ecosystems of continental climatic zone with high temperature contrasts.Front Microbiol2019;10:1573 PMCID:PMC6650587

[56]

Shannon CE. The mathematical theory of communication. Available from: https://pure.mpg.de/rest/items/item_2383164/component/file_2383163/content. [Last accessed on 27 Feb 2024]

[57]

Vainshtein BA. On some methods for assessing the similarity of biocenoses. Some Methods Assess Similarity Biocenoses 1976;46:981-6. (in Russian)

[58]

Praet J,Meeus I,Vandamme P.Gilliamella intestini sp. nov., Gilliamella bombicola sp. nov., Gilliamella bombi sp. nov. and Gilliamella mensalis sp. nov.: four novel Gilliamella species isolated from the bumblebee gut.Syst Appl Microbiol2017;40:199-204

[59]

Galac MR.Comparative pathology of bacteria in the genus Providencia to a natural host, Drosophila melanogaster.Microbes Infect2011;13:673-83 PMCID:PMC3109104

[60]

Kurtzman CP,Boekhout T. The yeasts: a taxonomic study. Elsevier; 2011. Available from: https://books.google.ru/books?hl=ru&lr=&id=yfg79rlIFIkC&oi=fnd&pg=PP2&ots=M0J-mwIryn&sig=dR-yEY7bsr-y7BLCvcRgG7iU0-s&redir_esc=y#v=onepage&q&f=false. [Last accessed on 27 Feb 2024]

[61]

Rattray FP. Cheese | Secondary cultures. In: Encyclopedia of dairy sciences. Elsevier; 2011. pp. 567-73. Available from: https://linkinghub.elsevier.com/retrieve/pii/B9780123744074000686. [Last accessed on 27 Feb 2024]

[62]

Koňuchová M.Modelling the radial growth of Geotrichum candidum: effects of temperature and water activity.Microorganisms2021;9:532 PMCID:PMC7999232

AI Summary AI Mindmap
PDF

98

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/