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A comparative study of gut microbiota profiles of earthworms fed in three different substrates

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Abstract

The gut microbiome of earthworms has a complex interdependence with the host. When the soil minerals pass through earthworm’s gut, they may affect the gut microbiota. To gain insight into the response of gut microbiota to the passed minerals, we fed earthworm (Eisenia fetida) on nutrient-poor soil and ore powder, and used high throughput sequencing to characterize the earthworm intestinal microbial community to find evidence for a core bacterial community of the E. fetida. The results showed that earthworms’ gut maintained a core microbiome that appeared in all samples. These core microbiota may play a significant role in a species’ environmental interactions. The composition of intestinal microbiomes varied with substrates. The earthworm guts from two nutrient-poor substrates had similar microbial communities and they were different from nutrient-rich substrate. Proteobacteria and Bacteroidetes were more abundant in the gut of earthworms kept on a nutrient-poor substrate such as ore powder or mineral soil than in the gut of earthworms kept in organic-rich compost soil; some of these microorganisms may help earthworms survive in nutrient-poor substrates.

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References

  • Aira M, Bybee S, Pérezlosada M, Domínguez J (2015) Feeding on microbiomes: effects of detritivory on the taxonomic and phylogenetic bacterial composition of animal manures. FEMS Microbiol Ecol 91:817–822

    Article  Google Scholar 

  • Aira M, Olcina J, Pérez-Losada M, Domínguez J (2016) Characterization of the bacterial communities of casts from Eisenia Andrei fed with different substrates. Appl Soil Ecol 98:103–111

    Article  Google Scholar 

  • Basker A, Kirkman JH, Macgregor AN (1994) Changes in potassium availability and other soil properties due to soil ingestion by earthworms. Biol Fertil Soils 17:154–158

    Article  CAS  Google Scholar 

  • Bokulich NA, Subramanian S, Faith JJ, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59. doi:10.1038/nmeth.2276

    Article  CAS  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byzov BA, Nechitaylo TY, Bumazhkin BK, Kurakov AV, Golyshin PN, Zvyagintsev DG (2009) Culturable microorganisms from the earthworm digestive tract. Microbiology 78:360–368

    Article  CAS  Google Scholar 

  • Byzov BA, Tikhonov VV, Nechitailo TY, Demin VV (2015) Taxonomic composition and physiological and biochemical properties of bacteria in the digestive tracts of earthworms. Eurasian Soil Science 48:268–275

    Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carpenter D, Hodson ME, Eggleton P, Kirk C (2007) Earthworm induced mineral weathering: preliminary results. Eur J Soil Biol 43:S176–S183

    Article  CAS  Google Scholar 

  • Colman DR, Toolson EC, Takacs-Vesbach CD (2012) Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol 21:5124–5137

    Article  CAS  PubMed  Google Scholar 

  • Dillon RJ, Dillon VM (2004) The gut bacteria of insects: nonpathogenic interactions. Entomology 49:71–92

    Article  CAS  Google Scholar 

  • Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards CA (2004) The importance of earthworms as key representatives of the soil fauna. In: Edwards CA (ed) Earthworm ecology, second edn. CRC Press, Boca Raton, pp 3–11

  • Edwards CA, Fletcher KE (1988) Interactions between earthworms and microorganisms in organic-matter breakdown. Agric Ecosyst Environ 24:235–247. doi:10.1016/0167-8809(88)90069-2

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Flint HJ, Scott KP, Louis P, Duncan SH (2012) The role of the gut microbiota in nutrition and health. Nat Rev Gastroenterol Hepatol 9:577–589

    Article  CAS  PubMed  Google Scholar 

  • Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, Bouffard GG, Blakesley RW, Murray PR, Green ED (2009) Topographical and temporal diversity of the human skin microbiome. Science 324:1190–1192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ, Castelle CJ, Butterfield CN, Hernsdorf AW, Amano Y, Ise K (2016) A new view of the tree of life. Nat Microbiol 1:16048

    Article  CAS  PubMed  Google Scholar 

  • Kersters K, De Vos P, Gillis M, Swings J, Vandamme P, Stackebrandt E (2006) Introduction to the Proteobacteria. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 3–37. doi:10.1007/0-387-30745-1_1

    Chapter  Google Scholar 

  • Kim HJ, Shin KH, Hur HG, Cha CJ (2004) Analysis of aerobic and Culturable bacterial community structures in earthworm (Eisenia fetida) intestine. J Appl Biol Chem 47:137–142

    CAS  Google Scholar 

  • Knapp BA, Seeber J, Podmirseg SM, Meyer E, Insam H (2008) Application of denaturing gradient gel electrophoresis for analysing the gut microflora of Lumbricus rubellus Hoffmeister under different feeding conditions. Bull Entomol Res 98:271–279

    Article  CAS  PubMed  Google Scholar 

  • Knapp BA, Podmirseg SM, Seeber J, Meyer E, Insam H (2009) Diet-related composition of the gut microbiota of Lumbricus rubellus as revealed by a molecular fingerprinting technique and cloning. Soil Biol Biochem 41:2299–2307

    Article  CAS  Google Scholar 

  • Kodama N, Kimura T, Yonemura S, Kaneda S, Ohashi M, Ikeno H (2014) Automated analysis of two-dimensional positions and body lengths of earthworms (Oligochaeta); MimizuTrack. PLoS One 9:e97986

    Article  PubMed  PubMed Central  Google Scholar 

  • Koubová A, Chroňáková A, Pižl V, Sánchez-Monedero MA, Elhottová D (2015) The effects of earthworms Eisenia spp. on microbial community are habitat dependent. Eur J Soil Biol 68:42–55

    Article  Google Scholar 

  • Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R (2008) Evolution of mammals and their gut microbes. Science 320:1647–1651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu D, Lian B, Wang B, Jiang G (2011) Degradation of potassium rock by earthworms and responses of bacterial communities in its gut and surrounding substrates after being fed with mineral. PLoS One 6:e28803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu DF, Lian B, Wang B (2016) Solubilization of potassium containing minerals by high temperature resistant Streptomyces sp.isolated from earthworm's gut. Acta Geochimica 35:262–270

    Article  CAS  Google Scholar 

  • Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L, Xie Y, Han Z, Giesy JP, Zhang X (2017) Responses of earthworms and microbial communities in their guts to Triclosan. Chemosphere 168:1194–1202. doi:10.1016/j.chemosphere.2016.10.079

    Article  CAS  PubMed  Google Scholar 

  • Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

    Article  PubMed  PubMed Central  Google Scholar 

  • Maslowski KM, Mackay CR (2011) Diet, gut microbiota and immune responses. Nat Immunol 12:5–9

    Article  CAS  PubMed  Google Scholar 

  • Needham SJ, Worden RH, McIlroy D (2004) Animal-sediment interactions: the effect of ingestion and excretion by worms on mineralogy. Biogeosciences 1:113–121

    Article  CAS  Google Scholar 

  • Pass DA (2015) The earthworm microbiome. Dissertation, Cardiff University

  • Plum NM, Filser J (2005) Floods and drought: response of earthworms and potworms (Oligochaeta: Lumbricidae, Enchytraeidae) to hydrological extremes in wet grassland. Pedobiologia 49:443–453. doi:10.1016/j.pedobi.2005.05.004

    Article  Google Scholar 

  • Rudi K, Odegård K, Løkken TT, Wilson R (2009) A feeding induced switch from a variable to a homogenous state of the earthworm gut microbiota within a host population. PLoS One 4:e7528

    Article  PubMed  PubMed Central  Google Scholar 

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A, Singh DP, Tiwari R, Kumar K, Singh RV, Singh S, Prasanna R, Saxena AK, Nain L (2015) Taxonomic and functional annotation of gut bacterial communities of Eisenia Foetida and Perionyx excavatus. Microbiol Res 175:48–56

    Article  CAS  PubMed  Google Scholar 

  • Sruthy PB, Anjana JC, Rathinamala J, Jayashree S (2013) Screening of earthworm (Eudrilus eugeniae) gut as a transient microbial habitat. Adv Zool Bot 1:53–56

    Google Scholar 

  • Thakuria D, Schmidt O, Finan D, Egan D, Doohan FM (2009) Gut wall bacteria of earthworms: a natural selection process. ISME J 4:357–366 http://www.nature.com/ismej/journal/v4/n3/suppinfo/ismej2009124s1.html

    Article  PubMed  Google Scholar 

  • Thakuria D, Schmidt O, Finan D, Egan D, Doohan FM (2010) Gut wall bacteria of earthworms: a natural selection process. ISME J 4:357–366

    Article  PubMed  Google Scholar 

  • Zhang W, Chen D, Zhao C (2007) Functions of earthworm in ecosystem biodiversity. Science 15:142–153

    CAS  Google Scholar 

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Acknowledgements

This work was supported by National Natural Science Foundation of China (U1204405 and 41373078) and Natural Science Foundation of Henan Educational Committee, China (14B180010).

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Authors and Affiliations

  1. Department of Bioengineering, Puyang Vocational and Technical College, Huanghe Road, Puyang, 457000, People’s Republic of China

    Dianfeng Liu, Chunhao Wu & Peijun Guo

  2. College of Life Sciences, Nanjing Normal University, No. 1, Wenyuan Road, Nanjing, 210046, People’s Republic of China

    Bin Lian

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  1. Dianfeng Liu
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  2. Bin Lian
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  3. Chunhao Wu
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  4. Peijun Guo
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Correspondence to Dianfeng Liu or Bin Lian.

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Liu, D., Lian, B., Wu, C. et al. A comparative study of gut microbiota profiles of earthworms fed in three different substrates. Symbiosis 74, 21–29 (2018). https://doi.org/10.1007/s13199-017-0491-6

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