Abstract
In this study, the aerobic activated sludge for skatole removal was enriched from pig slurry in three parallel sequencing batch reactors. The sludge system exhibited a satisfactory performance for skatole removal during the 40 days operation. High-throughput sequencing results showed that the α-diversity remained unchanged before and after the operation process. However, the structures of bacterial and fungal communities notably shifted. Particularly, Arthrobacter increased to be the major bacterial genus from 2.15 ± 0.76% (day 0) to 23.80 ± 24.36% (day 40), and Fusicolla became the major fungal genus from 1.20 ± 0.48% (day 0) to 37.17 ± 7.47% (day 40). These results indicated that Arthrobacter and Fusicolla might participate in skatole removal in sludge systems, though both genera were not reported to be able to degrade skatole. This is the first study describing skatole-degrading bacterial and fungal communities in the enrichment from pig slurry to the best of our knowledge, providing important guidance for skatole control and bioremediation.
This is a preview of subscription content, log in via an institution to check access.
Data availability
The raw sequence data have been deposited in the Genome Sequence Archive in BIG Data Center with accession number CRA002571.
References
Carlson JR, Yokoyama MT, Dickinson EO (1972) Induction of pulmonary edema and emphysema in cattle and goats with 3-methylindole. Science 176:298–299. https://doi.org/10.1126/science.176.4032.298
Feng K, Zhang Z, Cai W, Liu W, Xu M, Yin H, Wang A, He Z, Deng Y (2017) Biodiversity and species competition regulate the resilience of microbial biofilm community. Mol Ecol 26:6170–6182. https://doi.org/10.1111/mec.14356
Fu H, Wei Y, Zou Y, Li M, Wang F, Chen J, Zhang L, Liu Z, Ding L (2014) Research progress on the Actinomyces arthrobacter. Adv Microbiol 4:747–753. https://doi.org/10.4236/aim.2014.412081
Fukuoka K, Ozeki Y, Kanaly RA (2015) Aerobic biotransformation of 3-methylindole to ring cleavage products by Cupriavidus sp. strain KK10. Biodegradation 26:359–373. https://doi.org/10.1007/s10532-015-9739-0
Gräfenhan T, Schroers HJ, Nirenberg HI, Seifert KA (2011) An overview of the taxonomy, phylogeny, and typification of nectriaceous fungi in Cosmospora, Acremonium, Fusarium, Stilbella, and Volutella. Stud Mycol 68:79–113. https://doi.org/10.3114/sim.2011.68.04
Gu JD, Berry DF (1992) Metabolism of 3-methylindole by a methanogenic consortium. Appl Environ Microbiol 58:2667–2669. https://doi.org/10.1128/AEM.58.8.2667-2669.1992
Hughes DT, Pelletier J, Luetje CW, Leal WS (2010) Odorant receptor from the southern house mosquito narrowly tuned to the oviposition attractant skatole. J Chem Ecol 36:797–800. https://doi.org/10.1007/s10886-010-9828-9
Liu D, Wei Y, Liu X, Zhou Y, Jiang L, Yin J, Wang F, Hu Y, Nanjaraj Urs AN, Liu Y, Ang EL, Zhao S, Zhao H, Zhang Y (2018) Indoleacetate decarboxylase is a glycyl radical enzyme catalysing the formation of malodorant skatole. Nat Commun 9:4224. https://doi.org/10.1038/s41467-018-06627-x
Ma Q, Liu Z, Yang B, Dai C, Qu Y (2019) Characterization and functional gene analysis of a newly isolated indole-degrading bacterium Burkholderia sp. IDO3. J Hazard Mater 367:144–151. https://doi.org/10.1016/j.jhazmat.2018.12.068
Ma Q, Qu H, Meng N, Li S, Wang J, Liu S, Qu Y, Sun Y (2020) Biodegradation of skatole by Burkholderia sp. IDO3 and its successful bioaugmentation in activated sludge systems. Environ Res 182:109123. https://doi.org/10.1016/j.envres.2020.109123
Ma Q, Liu S, Li S, Hu J, Tang M, Sun Y (2020) Removal of malodorant skatole by two enriched microbial consortia: performance, dynamic, function prediction and bacteria isolation. Sci Total Environ 725:138416. https://doi.org/10.1016/j.scitotenv.2020.138416
Mackie RI, Stroot PG, Varel VH (1998) Biochemical identification and biological origin of key odor components in livestock waste. J Anim Sci 76:1331–1342. https://doi.org/10.2527/1998.7651331x
Meng X, He ZF, Li HJ, Zhao X (2013) Removal of 3-methylindole by lactic acid bacteria in vitro. Exp Ther Med 6:983–988. https://doi.org/10.3892/etm.2013.1251
Morales P, Cáceres M, Scott F, Díaz-Robles L, Aroca G, Vergara-Fernández A (2017) Biodegradation of benzo[α]pyrene, toluene, and formaldehyde from the gas phase by a consortium of Rhodococcus erythropolis and Fusarium solani. Appl Microbiol Biotechnol 101:6765–6777. https://doi.org/10.1007/s00253-017-8400-8
Sharma N, Doerner KC, Alok PC, Choudhary M (2015) Skatole remediation potential of Rhodopseudomonas palustris WKU-KDNS 3 isolated from an animal waste lagoon. Lett Appl Microbiol 60:298–306. https://doi.org/10.1111/lam.12379
Tesso TA, Zheng A, Cai H, Liu G (2019) Isolation and characterization of two Acinetobacter species able to degrade 3-methylindole. PLoS ONE 14:e0211275. https://doi.org/10.1371/journal.pone.0211275
Weems JM, Yost GS (2010) 3-Methylindole metabolites induce lung CYP1A1 and CYP2F1 enzymes by AhR and non-AhR mechanisms, respectively. Chem Res Toxicol 23:696–704. https://doi.org/10.1021/tx9004506
Yin B, Huang L, Gu JD (2006) Biodegradation of 1-methylindole and 3-methylindole by mangrove sediment enrichment cultures and a pure culture of an isolated Pseudomonas aeruginosa Gs. Water Air Soil Pollut 176:185–199. https://doi.org/10.1007/s11270-006-9159-1
Zhang Z, Zhao W, Xiao J et al (2019) Database resources of the BIG data center in 2019. Nucleic Acids Res 47:D8–D14. https://doi.org/10.1093/nar/gky993
Acknowledgements
The study was supported by the Fundamental Research Funds for the Central Universities (Nos. 3132020145 and 3132019335), and the Double First-Class Construction Fund of Dalian Maritime University (2020-cxxmss022).
Author information
Authors and Affiliations
Contributions
QH, MN and LS performed the experiments, data collection and statistical analysis. WJ and SY contributed suggestions. MQ designed the study, contributed to analyzing data, and wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest in the publication.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Qu, H., Meng, N., Liu, S. et al. Bacterial and fungal community compositions and structures of a skatole-degrading culture enriched from pig slurry. 3 Biotech 10, 471 (2020). https://doi.org/10.1007/s13205-020-02465-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-020-02465-1