Altered diversity of bacterial communities in two Drosophila species under laboratory conditions and lead exposure

Authors

  • Mirjana B. Beribaka Faculty of Technology, University of East Sarajevo, Karakaj 34A, 75400 Zvornik
  • Ivica Z. Dimkić Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade
  • Mihailo Đ. Jelić Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade
  • Slaviša M. Stanković Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade
  • Novo M. Pržulj Faculty of Agriculture, University of Banja Luka, Bulevar vojvode Petra Bojovića 1A, 78000 Banja Luka
  • Marko Lj. Anđelković Serbian Academy of Sciences and Arts, Kneza Mihaila 35, 11000 Belgrade
  • Marina M. Stamenković-Radak Faculty of Biology, University of Belgrade, Studentski trg 16, 11000 Belgrade

DOI:

https://doi.org/10.2298/ABS200911054B

Keywords:

Drosophila melanogaster, Drosophila subobscura, lead exposure, microbiota diversity, next-generation sequencing

Abstract

Paper description:

  • Changes in climatic and environmental parameters give relevance to the study of factors that shape the interactions between insects and microbiota, and to their adaptive significance.
  • Microbiota diversity in two Drosophila species from field-collected samples and their laboratory progeny with and without exposure to lead pollution is the first investigation of the bacterial communities associated with subobscura.
  • Significant species-specific differences in bacterial composition between populations and treatments was revealed. The diversity of bacterial communities increased in both species under lead exposure.
  • Increased microbiota diversity under lead pollution could serve as an indicator of the adaptive response to environmental stress.

Abstract: The composition of microbiota affects different traits of Drosophila throughout its life cycle and represents an important part of the adaptive response to environmental changes, such as increased levels of accumulated heavy metals in their habitats. We investigated the effects of lead added to the feeding substrate on the microbiota diversity in the fruit flies, Drosophila melanogaster and Drosophila subobscura. We compared the bacterial diversity of wild-caught flies and their progeny reared under standard laboratory conditions. We analyzed the shifts in bacterial diversity in the experimental groups of flies reared for 13 generations on standard and lead(II) acetate (Pb(CH3COO)2), Pb acetate-saturated substrates. Identification of the main bacterial genera was performed by next-generation sequencing (NGS) of the V3-V4 variable regions of the 16S rRNA gene. Results indicate significant species-specific differences in bacterial composition between natural and laboratory populations, and between the substrates. Diversity increased in both species under prolonged exposure to lead-polluted substrate, suggesting a potential adaptive response to an environmental stress.

Downloads

Download data is not yet available.

References

Ferrari J, Vavre F. Bacterial symbionts in insects or the story of communities affecting communities. Philos Trans R Soc Lond B Biol Sci. 2011;366(1569):1389-400.

Engel P, Moran NA. The gut microbiota of insects – diversity in structure and function. FEMS Microbiol Rev. 2013;37(5):699-735.

Rosshart SP, Vassallo BG, Angeletti D, Hutchinson DS, Morgan AP, Takeda K, Hickman HD, McCulloch JA, Badger JH, Ajami NJ, Trinchieri G, Pardo-Manuel de Villena F, Yewdell JW, Rehermann B. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell. 2017;171(5):1015-1028.e13.

Gould AL, Zhang V, Lamberti L, Jones EW, Obadia B, Korasidis N, Gavryushkin A, Carlson JM, Beerenwinkel N, Ludington WB. Microbiome interactions shape host fitness. Proc Natl Acad Sci U S A. 2018;115(51):e11951-60.

Bestion E, Jacob S, Zinger L, Di Gesu L, Richard M, White J, Cote J. Climate warming reduces gut microbiota diversity in a vertebrate ectotherm. Nat Ecol Evol. 2017;1(6):0161.

Erkosar B, Yashiro E, Zajitschek F, Friberg U, Maklakov AA, van der Meer JR, Kawecki TJ. Host diet mediates a negative relationship between abundance and diversity of Drosophila gut microbiota. Ecol Evol. 2018;8(18):9491-502.

Han G, Lee HJ, Jeong SE, Jeon CO, Hyun S. Comparative analysis of Drosophila melanogaster gut microbiota with respect to host strain, sex, and age. Microb Ecol. 2017;74(1):207-16.

Lu K, Abo RP, Schlieper KA, Graffam ME, Levine S, Wishnok JS, Swenberg JA, Tannenbaum SR, Fox JG. Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: An integrated metagenomics and metabolomics analysis. Environ Health Perspect. 2014;122(3):284-91.

Wu J, Wen XW, Faulk C, Boehnke K, Zhang H, Dolinoy DC, Xi C. Perinatal lead exposure alters gut microbiota composition and results in sex-specific bodyweight increases in adult mice. Toxicol Sci. 2016;151(2):324-33.

Zhang W, Guo R, Yang Y, Ding J, Zhang Y. Long-term effect of heavy-metal pollution on diversity of gastrointestinal microbial community of Bufo raddei. Toxicol Lett. 2016;258:192-7.

Stamenkovic-Radak M, Kalajdzic P, Savic T, Savic M, Kurbalija Z, Rasic G, Andjelkovic M. The effect of lead on fitness components and developmental stability in Drosophila subobscura. Acta Biol Hung. 2008;59(1):47-56.

Kenig B, Stamenković-Radak M, Andelković M. Population specific fitness response of Drosophila subobscura to lead pollution. Insect Sci. 2013;20(2):245-53.

Kalajdzic P, Kenig B, Andjelkovic M. Drosophila subobscura flies adapted to low lead concentration carry no fitness cost. Environ Pollut. 2015;204:90-8.

Mathew BB, Krishnamurthy NB. Assessment of lead toxicity using Drosophila melanogaster as a model. J Clin Toxicol. 2018;8(2):380.

Krimbas CB. Drosophila subobscura: biology, genetics and inversion polymorphism. 1st Ed. Hamburg: Dr Kovač; 1993.

Martinez D, Moya A, Latorre A, Fereres A. Mitochondrial DNA variation in Rhopalosiphum padi (Homoptera: Aphididae) populations from four Spanish localities. Ann Entomol Soc Am. 1992;85(2):241-6.

Kapun M, Barrón MG, Staubach F, Obbard DJ, Wiberg RAW, Vieira J, Goubert C, Rota-Stabelli O, Kankare M, Bogaerts-Márquez M, Haudry A, Waidele L, Kozeretska I, Pasyukova EG, Loeschcke V, Pascual M, Vieira CP, Serga S, Montchamp-Moreau C, et al. Genomic analysis of European Drosophila melanogaster populations reveals longitudinal structure, continent-wide selection, and previously unknown DNA viruses. Mol Biol Evol. 2020;37(9):2661-78.

Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M, Glöckner FO. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2013;41(1):e1.

Rosen MJ, Callahan BJ, Fisher DS, Holmes SP. Denoising PCR-amplified metagenome data. BMC Bioinformatics. 2012;13(1):283.

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581-3.

Callahan BJ, Sankaran K, Fukuyama JA, McMurdie PJ, Holmes SP. Bioconductor workflow for microbiome data analysis: from raw reads to community analyses. F1000Res. 2016;5:1492.

BBDuk Guide - DOE Joint Genome Institute [Internet]. DOE Joint Genome Institute. 2020 [cited 3 Sep 2020]. Available from: https://jgi.doe.gov/data-and-tools/bbtools/bb-tools-user-guide/bbduk-guide/.

Release 132 [Internet]. Arb-silva.de. 2020 [cited 3 September 2020]. Available from: https://www.arb-silva.de/documentation/release-132/

Wang Q, Garrity GM, Tiedje JM, Cole JR. Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol. 2007;73(16):5261-7.

Callahan B. Silva taxonomic training data formatted for DADA2 (Silva version 132) [Internet]. Zenodo. 2020 [cited 3 Sep 2020]. Available from: http://doi.org/10.5281/zenodo.1172783

Jelić M, Castro JA, Kurbalija Novičić Z, Kenig B, Dimitrijević D, Savić Veselinović M, Jovanović M, Milovanović D, Stamenković-Radak M, Andjelković M. Absence of linkage disequilibria between chromosomal arrangements and mtDNA haplotypes in natural populations of Drosophila subobscura from the Balkan Peninsula. Genome. 2012;55(3):214-21.

Erić P, Jelić M, Savić Veselinović M, Kenig B, Anđelković M, Stamenković-Radak M. Nucleotide diversity of Cyt b gene in Drosophila subobscura Collin. Genetika. 2019;51(1):213-26.

Staubach F, Baines JF, Künzel S, Bik EM, Petrov DA. Host species and environmental effects on bacterial communities associated with Drosophila in the laboratory and in the natural environment. PLoS One. 2013;8(8):e70749.

Capy P, Gibert P. Drosophila melanogaster, Drosophila simulans: so similar yet so different. Genetica. 2004;120(1-3):5-16.

Chandler JA, Morgan Lang J, Bhatnagar S, Eisen JA, Kopp A. Bacterial communities of diverse Drosophila species: ecological context of a host-microbe model system. PLoS Genet. 2011;7(9):e1002272.

Mamlouk D, Gullo M. Acetic Acid bacteria: physiology and carbon sources oxidation. Indian J Microbiol. 2013;53(4):377-84.

Chaston JM, Newell PD, Douglas AE. Metagenome-wide association of microbial determinants of host phenotype in Drosophila melanogaster. MBio. 2014;5(5):e01631-14.

Lee H-Y, Lee S-H, Lee J-H, Lee W-J, Min K-J. The role of commensal microbes in the lifespan of Drosophila melanogaster. Aging. 2019;11(13):4611-40.

Moreno J, Peinado R. Enological chemistry. Amsterdam: Elsevier Academic Press; 2012.

Nie Z, Zheng Y, Xie S, Zhang X, Song J, Xia M, Wang M. Unraveling the correlation between microbiota succession and metabolite changes in traditional Shanxi aged vinegar. Sci Rep. 2017;7(1):9240.

Galac MR, Lazzaro BP. Comparative pathology of bacteria in the genus Providencia to a natural host, Drosophila melanogaster. Microbes Infect. 2011;13(7):673-83.

Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA, Moran NA. Heritable endosymbionts of Drosophila. Genetics. 2006;174(1):363-76.

Werren JH, Windsor DM. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc R Soc London Ser B Biol Sci. 2000;267(1450):1277-85.

Kriesner P, Conner WR, Weeks AR, Turelli M, Hoffmann, AA. Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy. Evolution. 2016;70(5):979-97.

Wang L, Zhou C, He Z, Wang Z-G, Wang J-L, Wang Y-F. Wolbachia infection decreased the resistance of Drosophila to lead. PLoS One. 2012;7(3):e32643.

Xia J, Lu L, Jin C, Wang S, Zhou J, Ni Y, Fu Z, Jin Y. Effects of short term lead exposure on gut microbiota and hepatic metabolism in adult zebrafish. Comp Biochem Physiol Part C Toxicol Pharmacol. 2018;209:1-8.

Gupta P, Diwan B. Bacterial Exopolysaccharide mediated heavy metal removal: A Review on biosynthesis, mechanism and remediation strategies. Biotechnol Reports. 2017;13:58-71.

Downloads

Published

2021-03-19

How to Cite

1.
Beribaka MB, Dimkić IZ, Jelić M Đ., Stanković SM, Pržulj NM, Anđelković ML, Stamenković-Radak MM. Altered diversity of bacterial communities in two Drosophila species under laboratory conditions and lead exposure. Arch Biol Sci [Internet]. 2021Mar.19 [cited 2024Nov.25];73(1):17-29. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/6320

Issue

Vol. 73 No. 1 (2021)

Section

Articles

License

Copyright (c) 2021 Archives of Biological Sciences

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.