Abstract
Chironomids are the most abundant aquatic insects in freshwater habitats that can survive in extreme conditions. In this study, as the microbiome provides extended genotype to the host to perform various functions, we explored the microbiota of the Chironomus circumdatus larvae to find out the putative role played by the symbiotic bacteria for the host. The metabarcoding analyses of the larvae revealed that the insect harbors 1771 phylotypes. Out of the various microbial communities found, the majority corresponded to the phyla Proteobacteria (52.59%) and Actinobacteria (20.56%), respectively. The midges also harbored Klebsiella (2.57%), Enterobacter (1.32%), Bacillus (2.29%), and Acinetobacter (2.13%) genera that are involved in detoxification of xenobiotics present in the water. The presence of radiation-resistant genera like Deinococcus, including bacterial species like radiodurans, a highly radiation-resistant bacterium, indicates its potential to support the host’s ability to sustain in adverse environments. The functional profiling of the bacteria showed the relative abundance of many enzyme groups, such as transferases (40.62%), oxidoreductases (23.49%), and hydrolases (3.77%). The results indicate that the larvae harbor a considerable variety of bacteria that help the host adapt and survive in the polluted waters. The present study provides thorough insights into the microbiome of the C. circumdatus larvae that can be exploited for the bioremediation of certain pollutants through biomimetic strategies. It also gives us a wake-up call to take a good look at the guts of these disease-carrying insects’ inabilities to spread deadly human diseases.
Similar content being viewed by others
Data availability
All the data generated or analyzed during this study is provided in the manuscript and its associated materials.
Code availability
Not applicable.
References
Abo-Amer A (2011) Biodegradation of diazinon by Serratia marcescens DI101 and its use in bioremediation of contaminated environment. J Microbial Biotechnol 21: 71–80. PMID: 21301195. https://doi.org/10.4014/jmb.1007.07024
Abraham S, Silambarasan S, Logeswari P (2014) Simultaneous degradation of organophosphorus and organochlorine pesticides by bacterial consortium. J Taiwan Ins Chem Eng 45:2590–2596. https://doi.org/10.1016/j.jtice.2014.06.014
Abubacker N, Visvanathan M, Srinivasan S (2016) Biodegradation of glyphosate herbicide by bacterial isolates from banana (Musa spp.). Plantation Soil Biolife J 4:243–250. https://doi.org/10.17812/blj.2016.425
Ahemad M, Khan S (2010) Influence of selective herbicides on plant growth promoting traits of phosphate solubilizing Enterobacter asburiae strain PS2. Res J Microbiol 5:849–857. https://doi.org/10.3923/jm.2010.849.857
Ahire K, Balu K, Girish K, Yogesh S, Rajendra D (2012) Biodegradation of tributyl phosphate by novel bacteria isolated from enrichment cultures. Biodegradation 23:165–176. https://doi.org/10.1007/s10532-011-9496-7
Amann I, Ludwig W, Schleifer H (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Reviews 59:143–169. (PMID: 7535888)
Armitage P, Cranston S, Pinder V (1995) The Chironomidae: the biology and ecology of non-biting midges. Chapman & Hall ISBN-13:978–0412452604
Azambuja P, Garcia S, Ratcliffe A (2005) Gut microbiota and parasite transmission by insect vectors. Trends Parasitol 21:568–572. https://doi.org/10.1016/j.pt.2005.09.011. (PMID:16226491)
Azmy F, Saafan E, Essam M, Amin A, Ahmed H (2015) Biodegradation of malathion by Acinetobacter baumannii strain AFA isolated from domestic sewage in Egypt. Int J Biol Biomol Agri Food and Biotech Eng 9:54–65. https://doi.org/10.5281/zenodo.10991901/2011/805187. (PMID: 21912739)
Basset Y, Cizek L, Cuénoud P, Didham K, Guilhaumon F, Missa O, Novotny V, Odegaard F, Roslin T, Schmidl J, Tishechkin K, Winchester N, Roubik W, Aberlenc P, Bail J, Barrios H, Bridle R, Castaño-Meneses G, Corbara B, Curletti G, da Rocha D, de Bakker D, Delabie H, Dejean A, Fagan L, Floren A, Kitching L, Medianero E, Miller E, de Oliveira G, Orivel J, Pollet M, Rapp M, Ribeiro P, Roisin Y, Schmidt B, Sorensen L, Leponce M (2012) Arthropod diversity in a tropical forest. Science 338:1481–1484. https://doi.org/10.1126/science.1226727
Baumann P (2005) Biology bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189. https://doi.org/10.1146/annurev.micro.59.030804.121041. (PMID: 16153167)
Beunink J, Rehm J (1988) Synchronous anaerobic and aerobic degradation of DDT by an immobilized mixed culture system. Appl Microbiol Biotech 29:72–80. https://doi.org/10.1007/BF00258354
Bisthoven D, Janssens L, Nuyts P, Goddeeris B, Ollevier F (1998) Sublethal parameters in morphologically deformed Chironomus larvae: clues to understanding their bioindicator value. Freshwater Biol 39(1):179–191
Breznak A (2004) Invertebrates-insects. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM Press, Washington, D.C., pp 191–203
Broza M, Halpern M (2001) Chironomids egg masses and Vibrio cholerae. Nature 412:40. https://doi.org/10.1038/35083691
Brune A, Dietrich C (2015) The gut microbiota of termites: digesting the diversity in the light of ecology and evolution. Annu Rev Microbiol 69:145–166. https://doi.org/10.1146/annurev-micro-092412-155715. (PMID: 26195303)
Caporaso G, Kuczynski J, Stombaugh J, Bittinger K, Bushman D, Costello K, Fierer N, Peña G, Goodrich K, Gordon I, Huttley A, Kelley T, Knights D, Koenig E, Ley R, Lozupone C, McDonald D, Muegge B, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh P, Walters W, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. https://doi.org/10.1038/nmeth.f.303. (PMID: 20383131)
Chapman D (2006) Numbers of living species in Australia and the world. Australian Biol Resources Study. Canberra, Australia 61
Chen L, Siu K, Wu C, Shaio F, Huang Y, Fung P, Lee M, Cho L (2007) Comparison of one-tube multiplex PCR, automated ribotyping and intergenic spacer (ITS) sequencing for rapid identification of Acinetobacter baumannii. Clin Microbiol and Infect 13:801–806. https://doi.org/10.1111/j.1469-0691.2007.01744.x
Chen S, Luo J, Hu M, Lai K, Geng P, Huang H (2012) Enhancement of cypermethrin degradation by a coculture of Bacillus cereus ZH-3 and Streptomyces aureus HP-S-01. Bioresource Tech 110:97–104. https://doi.org/10.1016/j.biortech.2012.01.106
Corbi J, Bernegossi A, Moura L, Felipe M, Issa C, Silva M, Gorni G (2019) Chironomus sancticaroli (Diptera, Chironomidae) as a sensitive test species: can we rely on its use after repeated generations, under laboratory conditions? Bull Environ Contam Toxicol 103:213–217. https://doi.org/10.1007/s00128-019-02644-8
Curtis H, Rob K, Titus C, B, J Gregory C, Jose C, Dirk G, Eric A, Scott T, Dan K, Ruth E, Anup M (2014) Advancing the microbiome research community. Cell 159(2):227–230. https://doi.org/10.1016/j.cell.2014.09.022.PMCID:PMC4221798
Cycoń M, Żmijowska A, Wójcik M, Piotrowska-Seget Z (2013) Biodegradation and bioremediation potential of diazinon-degrading Serratia marcescens to remove other organophosphorus pesticides from soils. J Environ Manage 117:7–16. https://doi.org/10.1016/j.jenvman.2012.12.031
Dar M, Pawar K, Pandit R (2018) Prospecting the gut fluid of giant African landsnail, Achatina fulica for cellulose degrading bacteria. Int Biodeterior Biodegradation 126:103–111. https://doi.org/10.1016/j.ibiod.2017.10.006
Di Veroli A, Selvaggi R, Goretti E (2012) Chironomid mouthpart deformities as indicator of environmental quality: a case study in Lake Trasimeno (Italy). J Environ Monit 14:1473–1478. https://doi.org/10.1039/c2em10882h
Engel P, Moran A (2013) The gut microbiota of insects - diversity in structure and function. FEMS Microbiol Rev 37:699–735. https://doi.org/10.1111/1574-6976.12025
Figueras J, Beaz-Hidalgo R, Senderovich Y, Laviad S, Halpern M (2011) Re-identification of Aeromonas isolates from chironomid egg masses as the potential pathogenic bacteria Aeromonas aquariorum. Env Microbiol Rep 3:239–244. https://doi.org/10.1111/j.1758-2229.2010.00216
Franzenburg S, Walter J, Künzel S, Wang J, Baines F, Bosch G, Fraune S (2013) Distinct antimicrobial peptide expression determines host species-specific bacterial associations. PNAS 110:E3730–E3738. https://doi.org/10.1073/pnas.1304960110
Gagliardi B, Long S, Pettigrove V, Griffin P, Hoffmann A (2019) A re-evaluation of chironomid deformities as an environmental stress response: avoiding survivorship bias and testing non contaminant biological factors. Environ Toxicol Chem 38:1658–1667. https://doi.org/10.1002/etc.4446
Gendrin M, Christophides K (2013) The Anopheles mosquito microbiota and their impact on pathogen transmission. Anopheles Mosquitoes - New Insights into Malaria Vectors. https://doi.org/10.5772/55107
Gregory C, Christian L, William A, WaltersL CL, Peter T, Noah F, Rob K (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS 108:4516–4522. https://doi.org/10.1073/pnas.100008010
Halpern M, Broza Y, Mittler S, Arakawa E, Broza M (2004) Chironomid egg masses as a natural reservoir of Vibrio cholerae non-O1 and non-0139 in freshwater habitats. Microbial Ecol 47:341–349. https://doi.org/10.1007/s00248-003-2007-6. (PMID: 14681736)
Halpern M, Gancz H, Broza B, Kashi Y (2003) Vibrio cholera hemagglutinin/protease degrades chironomid egg masses. Appl Environ Microbiol 69:4200–4204. https://doi.org/10.1128/AEM.69.7
Halpern M, Landsberg O, Raats D, Rosenberg E (2007) Culturable and VBNC Vibrio cholera; interactions with chironomid egg masses and their bacterial population. Microbial Ecol 53:285–298. https://doi.org/10.1007/s00248-006-9094-0
Halpern M, Senderovich Y (2015) Chironomid microbiome. Microb Ecol 70(1):1–8. https://doi.org/10.1007/s00248-014-0536-9
Handelsman J, Rondon R, Brady F, Clardy J, Goodman M (1998) Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 5:R245–R249. https://doi.org/10.1016/s1074-5521(98)90108-9. (PMID: 9818143)
Healthcare-associated infections (HAI): diseases and organisms (2014) Centers for Dis Cont and Prevent. Pseudomonas aeruginosa in Healthcare Settings
Horner R (2010) Spontaneous bacterial peritonitis caused by Streptococcus bovis: case report and review of the literature. Brazilian J Inf Dis 14(3):294–296. https://doi.org/10.1590/S1413-86702010000300017
Huang Y, Xiao L, Li F et al (2018) Microbial degradation of pesticide residues and an emphasis on the degradation of cypermethrin and 3-phenoxy benzoic acid: a review Mol 23(9):2313. https://doi.org/10.3390/2Fmolecules23092313
Ifediegwu C, Agu C, Awah S, Mbachu E, Okeke B, Anaukwu G, Uba O, Ngenegbo C, Nwankwo M (2015) Isolation, growth and identification of Chlorpyrifos degrading bacteria from agricultural soil in Anambra State, Nigeria. Universal J of Microbiol Res 3:46–52. https://doi.org/10.13189/ujmr.2015.030402
Indiragandhi P, Anandham, R, Sa M (2011). Functional significance of insect gut bacteria and their role in host insect processes, development, and crop production. In: Maheshwari, D. (eds) Bacteria in Agrobiology: Plant Growth Responses. https://doi.org/10.1007/978-3-642-20332-9_14
Jabeen H, Iqbal S, Anwar S, Parales E (2015) Optimization of profenofos degradation by a novel bacterial consortium PBAC using response surface methodology. Int Biodeter and Biodegrad 100:89–97. https://doi.org/10.1016/j.ibiod.2015.02.022
Jones R, Sanchez L, Fierer N (2013) Cross-taxon analysis of insect-associated bacterial diversity. PLoS ONE 8:e61218
Karigar S, Rao S (2011). Role of microbial enzymes in the bioremediation of pollutants: a review Enz Res 11. https://doi.org/10.4061/2011/805187. (PMID: 21912739)
Klein S, Recco A, Catalano T, Edberg C, Casey I, Steigbigel H (1977) Association of Streptococcus bovis with carcinoma of the colon. New England J of Med 297(15):800–802. https://doi.org/10.1056/NEJM197710132971503. (PMID: 408687)
Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Nat Acad Sci USA 108: 19288–19292. PMID: 22084077. https://doi.org/10.1073/pnas.1110474108
Krisko A, Radman M (2013) Biology of extreme radiation resistance: the way of Deinococcus radiodurans. Cold Spring Harb Perspect Biol 5(7):a012765. https://doi.org/10.1101/cshperspect.a012765
Kryuchkova V, Burygin L, Gogoleva E, Gogolev V, Chernyshova P, Makarov E, Fedorov E, Turkovskaya V (2014) Isolation and characterization of a glyphosate-degrading rhizosphere strain, Enterobacter cloacae K7. Microbiol Res 169:99–105. PMID: 23545355. https://doi.org/10.1016/j.micres.2013.03.002
Kulkarni V, Markad L, Melo S, D’Souza F, Kodam M (2014) Biodegradation of tributyl phosphate using Klebsiella pneumoniae sp. S3. Appl Microbiol Biotech 98:919–929. https://doi.org/10.1007/s00253-013-4938-2. (PMID: 23644771)
Kumar D, Ramesh U (2014) Rearing practices of live feedstuff animal midge fly larvae (Chironomus circumdatus) Kieffer (Diptera: Chironomidae). Int J Curr Sci 12:170–177
Kwon S, Sohn Y, Shin S, Kim E, Seo I (2005) Biodegradation of the organochlorine insecticide, endosulfan, and the toxic metabolite, endosulfan sulfate, by Klebsiella oxytoca KE-8. Appl Microbiol Biotech 67:845–850. https://doi.org/10.1007/s00253-004-1879-9. (PMID: 15700124)
Laviad-Shitrit S, Sharaby Y, Sela R, Thorat L, Nath B, Halpern M (2021) Copper and chromium exposure affect chironomid larval microbiota composition. Sci Total Environ 771:145330
Longkumer T, Parthasarathy S, Vemuri G, Siddavattam D (2014) OxyR-dependent expression of A. funestusa novel glutathione S-transferase (Abgst01) gene in Acinetobacter baumannii DS002 and its role in biotransformation of organophosphate insecticides. Microbiol 160:102–112. https://doi.org/10.1099/mic.0.070664-0
Maghdu A, Meera V, Sivagami S (2016) Biodegradation of glyphosate herbicide by bacterial isolates from banana (Musa spp.). Plantation soil Biolife J 4:243–250. Corpus ID: 212539032
Maleeka B, Rajesh G, Ram N (2016) Isolation, characterization and identification of dimethoate degrading bacteria from soil series of Tamil Nadu. Int J of Advan Scientific and Tech Res 3:220–230. Corpus ID: 212448994
Martinez E, Moore B, Schaumloffel J, Dasgupta N (2006) Morphologic and growth responses in Chironomus tentans to arsenic exposure. Arch Environ Contam Toxicol 51:529–536. https://doi.org/10.1007/s00244-005-0308-0
Meer W, Vos S, Harayama A, Zehnder (1992) Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol Rev 56(4):677–694. PMCID: PMC372894. PMID: 1480115
Merck Veterinary Manual (2008) “Subacute ruminal acidosis".
Mikaelyan A, Dietrich C, Köhler T, Poulsen M, Sillam-Dussès D, Brune A (2015) Diet is the Primary Determinant of Bacterial Community Structure in the Guts of Higher Termites. https://doi.org/10.1111/mec.13376
Minard G, Mavingui P, Moro V (2013) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasit Vectors 6:146. https://doi.org/10.1186/1756-3305-6-146. (PMID: 23688194)
Mohamed K, Ahmed A, Fetyan A, Elnagdy M (2010) Isolation and molecular characterisation of malathion-degrading bacterial strains from waste water in Egypt. J of Advan Res 1:145–149. https://doi.org/10.1016/j.jare.2010.03.007
Nartey R, Owusu-Dabo E, Kruppa T, Baffour-Awuah S, Annan A, Oppong S, Becker N, Obiri-Danso K (2013) Use of Bacillus thuringiensis varisraelensis as a viable option in an integrated malaria vector control programme in the Kumasi Metropolis. Ghana Parasit Vectors 6:116. https://doi.org/10.1186/1756-3305-6-116. (PMID: 23607376)
Ng F, Willner L, Lim W, Schmieder R, Chau B, Nilsson C, Anthony S, Ruan Y, Rohwer F, Breitbart M (2011) Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS ONE 6:e20579. https://doi.org/10.1371/journal.pone.0020579. (PMID: 21674005)
Novais C, Thorstenson R (2011) The evolution of Pyrosequencing® for microbiology: from genes to genomes. J Microbiol Methods 86(1):1–7. https://doi.org/10.1016/j.mimet.2011.04.006. (PMID: 21514329)
Phugare S, Kalyani C, Gaikwad B, Jadhav P (2013) Microbial degradation of imidacloprid and toxicological analysis of its biodegradation metabolites in silkworm (Bombyx mori). Chem Eng J 230:27–35. https://doi.org/10.1016/j.cej.2013.06.042
Pinder L (1986) Biology of freshwater chironomidae. Ann Rev Entomol 31:1–23
Ramprasad K, Thiyagarajan S, Puneeth K, Sreenath P, Ravi N, Tha T, Gopireddy V, Subba R (2017) Bacterial fauna associating with chironomid larvae from lakes of Bengaluru city, India - a 16s rRNA gene based identification. Genomics Data 12:44–48. https://doi.org/10.1016/j.gdata.2017.03.001
Ryan J, Ray C (2004) Sherris Med. Micro. (4th ed.). McGraw Hill. ISBN 0–8385–8529–9
Salmelin J, Vuori M, Hamalinen H (2015) Inconsistency in the analysis of morphological deformities in chironomidae (Insecta: Diptera) larvae. Env Toxicol Chem 34(8):1891–1898. https://doi.org/10.1002/etc.3010. (PMID: 26061223)
Schloss P, Westcott S, Ryabin T, Hall R, Hartmann M, Hollister B, Lesniewski A, Oakley B, Parks H, Robinson J, Sahl W, Stres B, Thallinger G, Van Horn J, Weber F (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. https://doi.org/10.1128/AEM.01541-09. (PMID: 19801464)
Schloss P, Kozich J, Westcott S, Baxter N, Highlander S (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79(17):5112–5120
Schowanek D, Verstraete W (1990) Phosphonate utilization by bacterial cultures and enrichments from environmental samples. Appl Environ Microbiol 56: 895–903. PMID: 2339877. PMCID: PMC184318
Sela R, Halpern M (2019) Seasonal dynamics of Chironomus transvaalensis populations and the microbial community composition of their egg masses. FEMS Microbiol Lett 366
Sela R, Hammer B, Halpern M (2020a) Quorum-sensing signaling by chironomid egg masses microbiota, affect haemagglutinin/protease (HAP) production by Vibrio cholerae. Mol Ecol. https://doi.org/10.1111/mec.15662
Sela R, Laviad-Shitrit S, Halpern M (2020b) Changes in microbiota composition along the metamorphosis developmental stages of Chironomus transvaalensis. Front Microbiol 11
Sela R, Laviad-Shitrit S, Thorat L, Nath, B, Halpern M (2021) Chironomus ramosus larval microbiome composition provides evidence for the presence of detoxifying enzymes. Microorganisms 9:1571. https://doi.org/10.3390/microorganisms9081571
Senderovich Y, Gershtein Y, Halewa E, Halpern M (2008) Vibrio cholerae and Aeromonas; do they share a mutual host? ISME J 2:276–283. https://doi.org/10.1038/ismej.2007.114. (PMID: 18317460)
Senderovich Y, Halpern M (2012) Bacterial community composition associated with chironomid egg masses. J Insect Sci 12:149. https://doi.org/10.1673/031.012.14901. (PMID: 23461272)
Shaha C, Pandit R (2021) Characterization of an esterase producing bacterium from the gut of Chironomus circumdatus (bloodworms) and its ability to use modified phthalates. Curr Microbiol. https://doi.org/10.1007/s00284-021-02574-x
Silva G, Green K, Dutilh B, Edwards R (2016) SUPER-FOCUS: a tool for agile functional analysis of shotgun metagenomic data. Bioinformatics 32(3):354–361. https://doi.org/10.1093/bioinformatics/btv584
Singh B, Kaur J, Singh K (2012) Biodegradation of malathion by Brevibacillus sp. strain KB2 and Bacillus cereus strain PU. World J of Microbiol Biotech 28:1133–1141. https://doi.org/10.1007/s11274-011-0916-y. (PMID: 22805834)
Surekha R, Vijaya Lakshmi D, Jaya M, Aruna, Jyothi, Narasimha, Venkateswarlu K (2008) Isolation and characterization of a chlorpyrifos-degrading bacterium from agricultural soil and its growth response. 342DF0310978(2):26–31. https://doi.org/10.5897/AJMR.9000447
Toft C, Andersson G (2010) Evolutionary microbial genomics: insights into bacterial host adaptation. Nat Rev Genet 11:465–475. PMID: 20517341. https://doi.org/10.1038/nrg2798
Vidya C, Kumar M, Khanna S (2008) Biotransformation of chlorpyrifos and bioremediation of contaminated soil. Int Biodeterioration and Biodegrad 62:204–209. https://doi.org/10.1016/j.ibiod.2007.12.005
Walker R (2001) Midges: Chironomidae and Related Diptera. In: Smol J.P., Birks H.J.B., Last W.M. (eds) Tracking environmental change using lake sediments. Developments in Paleoenvironmental Research 4. https://doi.org/10.1007/0-306-47671-1_3
Weiss B, Aksoy S (2011) Microbiome influences on insect host vector competence. Trends Parasitol 27:514–522. https://doi.org/10.1016/j.pt.2011.05
Zeinat M, Nashwa H, Fetyan A, Ibrahim A, El-Nagdy S (2008) Biodegradation and detoxification of malathion by of Bacillus thuringiensis MOS-5. Australian J of Basic and Applied Sci 2: 724–732. ISSN 1991–8178
Acknowledgements
Authors are also thankful to the Department of Zoology, Savitribai Phule Pune University for providing the infrastructure. Funding for the research work was supported by University Grant Commission (UGC)-Centre for Advanced Studies (Phase 3) (2019-2020) and Council of Scientific and Industrial Research (CSIR).This work is part of PhD thesis of Miss Chaitali Shaha.
Funding
The research work was supported by the University Grant Commission (UGC) Centre for Advanced Studies (Phase 3) (2019–2020) and Council of Scientific and Industrial Research (CSIR). No financial help was provided for publishing this article.
Author information
Authors and Affiliations
Contributions
Conceptualization: CMS; formal analysis: CMS; investigation: CMS; writing-original draft preparation: CMS, MAD; writing-review and editing: RSP, MAD; supervision: RSP. All authors have read and agreed to the final version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
This article does not contain any studies with human participants performed by any of the authors.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shaha, C.M., Dar, M.A. & Pandit, R.S. Mining the diversity and functional profile of bacterial symbionts from the larvae of Chironomus circumdatus (bloodworms). Folia Microbiol 67, 861–872 (2022). https://doi.org/10.1007/s12223-022-00984-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-022-00984-3