Abstract
Magnetotactic bacteria(MTB) display magnetotaxis ability because of biomineralization of intracellular nanometer-sized, membrane-bound organelles termed magnetosomes. Despite having been discovered more than half a century, only a few representatives of MTB have been isolated and cultured in the laboratory. In this study, we report the genomic characterization of a novel marine magnetotactic spirillum strain SH-1 belonging to the genus Terasakiella that was recently isolated. A gene encoding haloalkane dehalogenase, which is involved in the degradation of chlorocyclohexane, chlorobenzene, chloroalkane, and chloroalkene, was identified. SH-1 genome contained cysCHI and soxBAZYX genes, thus potentially capable of assimilatory sulfate reduction to H 2 S and using thiosulfate as electron donors and oxidizing it to sulfate. Genome of SH-1 also contained genes encoding periplasmic dissimilatory nitrate reductases(napAB), assimilatory nitrate reductase(nasA) and assimilatory nitrite reductases(nasB), suggesting that it is capable of gaining energy by converting nitrate to ammonia. The pure culture of Terasakiella sp. SH-1 together with its genomic results offers new opportunities to examine biology, physiology, and biomineralization mechanisms of MTB.
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Data Availability Statement
All data generated and analyzed during the current study are available from the corresponding author upon request.
References
Altschul S F, Gish W, Miller W, Myers E W, Lipman D J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215(3): 403–410, https://doi.org/10.1016/S0022-2836(05)80360-2.
Apweiler R, Bairoch A, Wu C H, Barker W C, Boeckmann B, Ferro S, Gasteiger E, Huang H Z, Lopez R, Magrane M, Martin M J, Natale D A, O’Donovan C, Redaschi N, Yeh L S L. 2004. UniProt: the Universal Protein knowledgebase. Nucleic Acids Research, 32(S1): D115–D119, https://doi.org/10.1093/nar/gkh131.
Arndt D, Grant J R, Marcu A, Sajed T, Pon A, Liang Y J, Wishart D S. 2016. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Research, 44(W1): W16–W21, https://doi.org/10.1093/nar/gkw387.
Ashburner M, Ball C A, Blake J A, Botstein D, Butler H, Cherry J M, Davis A P, Dolinski K, Dwight S S, Eppig J T, Harris M A, Hill D P, Tarver L I, Kasarskis A, Lewis S, Matese J C, Richardson J E, Ringwald M, Rubin G M, Sherlock G. 2000. Gene Ontology: tool for the unification of biology. Nature Genetics, 25(1): 25–29, https://doi.org/10.1038/75556.
Bazylinski D A, Blakemore R P. 1983. Denitrification and assimilatory nitrate reduction in Aquaspirillum magnetotacticum. Appl ied and Environ mental Microbiol ogy, 46(5): 1118–1124, https://doi.org/10.1128/AEM.46.5.1118-1124.1983.
Bazylinski D A, Frankel R B, Heywood B R, Mann S, King J W, Donaghay P L, Hanson A K. 1995. Controlled biomineralization of magnetite(Fe3O4) and greigite(Fe3S4) in a magnetotactic bacterium. Applied and Environmental Microbiology, 61: 3232–3239, https://doi.org/10.1128/AEM.61.9.3232-3239.1995.
Bazylinski D A, Frankel R B. 2004. Magnetosome formation in prokaryotes. Nature Reviews Microbiology, 2(3): 217–230, https://doi.org/10.1038/nrmicro842.
Bazylinski D A, Williams T J, Lefèvre C T, Trubitsyn D, Fang J S, Beveridge T J, Moskowitz B M, Ward B, Schübbe S, Dubbels B L, Simpson B. 2013. Magnetovibrio blakemorei gen. nov., sp. nov., a magnetotactic bacterium (Alphaproteobacteria: Rhodospirillaceae) isolated from a salt marsh. International Journal of Systematic and Evolutionary Microbiology, 63(Pt 5): 1824–1833, https://doi.org/10.1099/ijs.0.044453-0.
Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Research, 27(2): 573–580, https://doi.org/10.1093/nar/27.2.573.
Blakemore R P, Maratea D, Wolfe R S. 1979. Isolation and pure culture of a freshwater magnetic spirillum in chemically defined medium. Journal of Bacteriology, 140(2): 720–729, https://doi.org/10.1128/JB.140.2.720-729.1979.
Blakemore R P. 1982. Magnetotactic bacteria. Annual Review of Microbiology, 36: 217–238, https://doi.org/10.1146/annurev.mi.36.100182.001245.
Canchaya C, Proux C, Fournous G, Bruttin A, Brüssow H. 2003. Prophage genomics. Microbiology and Molecular Biology Reviews, 67(2): 238–276, https://doi.org/10.1128/mmbr.67.2.238-276.2003.
Casjens S. 2003. Prophages and bacterial genomics: what have we learned so far? Molecular Microbiology, 49(2): 277–300, https://doi.org/10.1046/j.1365-2958.2003.03580.x.
Consortium U P. 2015. UniProt: a hub for protein information. Nucleic Acids Research, 43(D1): D204–D212, https://doi.org/10.1093/nar/gku989.
DeLong E F, Frankel R B, Bazylinski D A. 1993. Multiple evolutionary origins of magnetotaxis in bacteria. Science, 259(5096): 803–806, https://doi.org/10.1126/science.259.5096.803.
Du H J, Zhang W Y, Zhang W S, Zhang W J, Pan H M, Pan Y X, Bazylinski D A, Wu L F, Xiao T, Lin W. 2019. Magnetosome gene duplication as an important driver in the evolution of magnetotaxis in the Alphaproteobacteria. mSystems, 4(5): e00315–19, https://doi.org/10.1128/mSystems.00315-19.
Fouts D E. 2006. Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Research, 34(20): 5839–5851, https://doi.org/10.1093/nar/gkl732.
Galperin M Y, Makarova K S, Wolf Y I, Koonin E V. 2015. Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Research, 43(D1): D261–D269, https://doi.org/10.1093/nar/gku1223.
Geurink C, Lefèvre C T, Monteil C L, Morillo-Lopez V, Abreu F, Bazylinski D A, Trubitsyn D. 2020. Complete genome sequence of strain BW-2, a magnetotactic gammaproteobacterium in the family Ectothiorhodospiraceae, isolated from a brackish spring in Death Valley, California. Microbiology Resource Announcements, 9(1): e01144–19, https://doi.org/10.1128/MRA.01144-19.
Grissa I, Vergnaud G, Pourcel C. 2007. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Research, 35(S2): W52–W57, https://doi.org/10.1093/nar/gkm360.
Grünberg K, Wawer C, Tebo B M, Schüler D. 2001. A large gene cluster encoding several magnetosome proteins is conserved in different species of magnetotactic bacteria. Applied and Environmental Microbiology, 67(10): 4573–4582, https://doi.org/10.1128/aem.67.10.4573-4582.2001.
Hanzlik M, Winklhofer M, Petersen N. 2002. Pulsed-fieldremanence measurements on individual magnetotactic bacteria. Journal of Magnetism and Magnetic Materials, 248(2): 258–267, https://doi.org/10.1016/S0304-8853(02)00353-0.
Hensen D, Sperling D, Trüper H G, Brune D C, Dahl C. 2006. Thiosulphate oxidation in the phototrophic sulphur bacterium Allochromatium vinosum. Molecular Microbiology, 62(3): 794–810, https://doi.org/10.1111/j.1365-2958.2006.05408.x.
Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D, Walter M C, Rattei T, Mende D R, Sunagawa S, Kuhn M, Jensen L J, von Mering C, Bork P. 2016. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Research, 44(D1): D286–D293, https://doi.org/10.1093/nar/gkv1248.
Janssen D B, Pries F, van der Ploeg J, Kazemier B, Terpstra P, Witholt B. 1989. Cloning of 1,2-dichloroethane degradation genes of Xanthobacter autotrophicus GJ10 and expression and sequencing of the dhlA gene. Journal of Bacteriology, 171(12): 6791–6799, https://doi.org/10.1128/jb.171.12.6791-6799.1989.
Ji B Y, Zhang S D, Arnoux P, Rouy Z, Alberto F, Philippe N, Murat D, Zhang W J, Rioux J B, Ginet N, Sabaty M, Mangenot S, Pradel N, Tian J S, Yang J, Zhang L C, Zhang W Y, Pan H M, Henrissat B, Coutinho P M, Li Y, Xiao T, Médigue C, Barbe V, Pignol D, Talla E, Wu L F. 2014. Comparative genomic analysis provides insights into the evolution and niche adaptation of marine Magnetospira sp. QH-2 strain. Environ mental Microbiol ogy, 16(2): 525–544, https://doi.org/10.1111/1462-2920-12180.
Ji B Y, Zhang S D, Zhang W J, Rouy Z, Alberto F, Santini C L, Mangenot S, Gagnot S, Philippe N, Pradel N, Zhang L C, Tempel S, Li Y, Médigue C, Henrissat B, Coutinho P M, Barbe V, Talla E, Wu L F. 2017. The chimeric nature of the genomes of marine magnetotactic coccoid-ovoid bacteria defines a novel group of Proteobacteria. Environ mental Microbiol ogy, 19(3): 1103–1119, https://doi.org/10.1111/1462-2920.13637.
Jogler C, Schüler D. 2009. Genomics, genetics, and cell biology of magnetosome formation. Annual Review of Microbiology, 63: 501–521, https://doi.org/10.1146/annurev.micro.62.081307.162908.
Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. 2016. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Research, 44(D1): D457–D462, https://doi.org/10.1093/nar/gkv1070.
Kolinko S, Jogler C, Katzmann E, Wanner G, Peplies J, Schüler D. 2012. Single-cell analysis reveals a novel uncultivated magnetotactic bacterium within the candidate division OP3. Environmental Microbiology, 14(7): 1709–1721, https://doi.org/10.1111/j.1462-2920.2011.02609.x.
Kuypers M M M, Marchant H K, Kartal B. 2018. The microbial nitrogen-cycling network. Nature Reviews Microbiology, 16(5): 263–276, https://doi.org/10.1038/nrmicro.2018.9.
Lefèvre C T, Abreu F, Schmidt M L, Lins U, Frankel R B, Hedlund B P, Bazylinski D A. 2010. Moderately thermophilic magnetotactic bacteria from hot springs in Nevada. Applied and Environmental Microbiology, 76(11): 3740–3743 https://doi.org/10.1128/AEM.03018-09.
Lefèvre C T, Bazylinski D A. 2013. Ecology, diversity, and evolution of magnetotactic bacteria. Microbiology and Molecular Biology Reviews, 77(3): 497–526, https://doi.org/10.1128/MMBR.00021-13.
Lefèvre C T, Bernadac A, Yu-Zhang K, Pradel N, Wu L F. 2009. Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environmental Microbiology, 11(7): 1646–1657, https://doi.org/10.1111/j.1462-2920.2009.01887.x.
Li Y J, Katzmann E, Borg S, Schüler D. 2012. The periplasmic nitrate reductase nap is required for anaerobic growth and involved in redox control of magnetite biomineralization in Magnetospirillum gryphiswaldense. J ournal of Bacteriol ogy, 194(18): 4847–4856, https://doi.org/10.1128/JB.00903-12.
Lin W, Pan Y X, Bazylinski D A. 2017a. Diversity and ecology of and biomineralization by magnetotactic bacteria. Environmental Microbiology Rep orts, 9(4): 345–356, https://doi.org/10.1111/1758-2229.12550.
Lin W, Pan Y X. 2015. A putative greigite-type magnetosome gene cluster from the candidate phylum Latescibacteria. Environ mental Microbiol ogy Rep orts, 7(2): 237–242, https://doi.org/10.1111/1758-2229.12234.
Lin W, Paterson G A, Zhu Q Y, Wang Y Z, Kopylova E, Li Y, Knight R, Bazylinski D A, Zhu R X, Kirschvink J L, Pan Y X. 2017b. Origin of microbial biomineralization and magnetotaxis during the Archean. Proceedings of the National Academy of Sciences of the United States of America, 114(9): 2171–2176, https://doi.org/10.1073/pnas.1614654114.
Lin W, Zhang W S, Paterson G A, Zhu Q Y, Zhao X, Knight R, Bazylinski D A, Roberts A P, Pan Y X. 2020. Expanding magnetic organelle biogenesis in the domain Bacteria. Microbiome, 8(1): 152, https://doi.org/10.1186/s40168-020-00931-9.
Lin W, Zhang W S, Zhao X, Roberts A P, Paterson G A, Bazylinski D A, Pan Y X. 2018. Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution. The ISME Journal, 12(6): 1508–1519, https://doi.org/10.1038/s41396-018-0098-9.
Lohße A, Ullrich S, Katzmann E, Borg S, Wanner G, Richter M, Voigt B, Schweder T, Schüler D. 2011. Functional analysis of the magnetosome island in Magnetospirillum gryphiswaldense: the mamAB operon is sufficient for magnetite biomineralization. PLoS One, 6(10): e25561, https://doi.org/10.1371/journal.pone.0025561.
Makarova K S, Wolf Y I, Koonin E V. 2015. Archaeal clusters of orthologous genes(arcogs): an update and application for analysis of shared features between thermococcales, methanococcales, and methanobacteriales. Life, 5(1): 818–840, https://doi.org/10.3390/life5010818.
Maratea D, Blakemore R P. 1981. Aquaspirillum magnetotacticum sp. nov., a magnetic spirillum. International Journal of Systematic and Evolutionary Microbiology, 31(4): 452–455, https://doi.org/10.1099/00207713-31-4-452.
Matsunaga T, Okamura Y, Fukuda Y, Wahyudi A T, Murase Y, Takeyama H. 2005. Complete genome sequence of the facultative anaerobic magnetotactic bacterium Magnetospirillum sp. strain AMB-1. DNA Research, 12(3): 157–166, https://doi.org/10.1093/dnares/dsi002.
Matsunaga T, Sakaguchi T, Tadakoro F. 1991. Magnetite formation by a magnetic bacterium capable of growing aerobically. Applied Microbiology and Biotechnology, 35(5): 651–655, https://doi.org/10.1007/BF00169632.
Matsunaga T, Tsujimura N. 1993. Respiratory inhibitors of a magnetic bacterium Magnetospirillum sp. AMB-1 capable of growing aerobically. Applied Microbiology and Biotechnology, 39(3): 368–371, https://doi.org/10.1007/BF00192094.
Miele V, Penel S, Duret L. 2011. Ultra-fast sequence clustering from similarity networks with SiLiX. BMC Bioinformatics, 12: 116, https://doi.org/10.1186/1471-2105-12-116.
Monteil C L, Perrière G, Menguy N, Ginet N, Alonso B, Waisbord B, Cruveiller S, Pignol D, Lefèvre C T. 2018. Genomic study of a novel magnetotactic Alphaproteobacteria uncovers the multiple ancestry of magnetotaxis. Environ mental Microbiol ogy, 20(12): 4415–4430, https://doi.org/10.1111/1462-2920.14364.
Murat D, Quinlan A, Vali H, Komeili A. 2010. Comprehensive genetic dissection of the magnetosome gene island reveals the step-wise assembly of a prokaryotic organelle. Proceedings of the National Academy of Sciences of the United States of America, 107(12): 5593–5598, https://doi.org/10.1073/pnas.0914439107.
Paul J H. 2008. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? The ISME Journal, 2(6): 579–589, https://doi.org/10.1038/ismej.2008.35.
Pinto R, Tang Q X, Britton W J, Leyh T S, Triccas J A. 2004. The Mycobacterium tuberculosis cysD and cysNC genes form a stress-induced operon that encodes a tri-functional sulfate-activating complex. Microbiology, 150(6): 1681–1686, https://doi.org/10.1099/mic.0.26894-0.
Richter M, Kube M, Bazylinski D A, Lombardot T, Glöckner F O, Reinhardt R, Schüler D. 2007. Comparative genome analysis of four magnetotactic bacteria reveals a complex set of group-specific genes implicated in magnetosome biomineralization and function. J ournal of Bacteriol ogy, 189(13): 4899–4910, https://doi.org/10.1128/JB.00119-07.
Rioux J B, Philippe N, Pereira S, Pignol D, Wu L F, Ginet N. 2010. A second actin-like MamK protein in Magnetospirillum magneticum AMB-1 encoded outside the genomic magnetosome island. PLoS One, 5(2): e9151, https://doi.org/10.1371/journal.pone.0009151.
Sakaguchi T, Arakaki A, Matsunaga T. 2002. Desulfovibrio magneticus sp. nov., a novel sulfate-reducing bacterium that produces intracellular single-domain-sized magnetite particles. International Journal of Systematic and Evolutionary Microbiology, 52(Pt 1): 215–221, https://doi.org/10.1099/00207713-52-1-215.
Schleifer K H, Schüler D, Spring S, Weizenegger M, Amann R, Ludwig W, Köhler M. 1991. The genus Magnetospirillum gen. nov. description of Magnetospirillum gryphiswaldense sp. nov. and transfer of Aquaspirillum magnetotacticum to Magnetospirillum magnetotacticum comb. nov. 1. Systematic and Applied Microbiology, 14(4): 379–385, https://doi.org/10.1016/s0723-2020(11)80313-9.
Schübbe S, Williams T J, Xie G, Kiss H E, Brettin T S, Martinez D, Ross C A, Schüler D, Cox B L, Nealson K H, Bazylinski D A. 2009. Complete genome sequence of the chemolithoautotrophic marine magnetotactic coccus strain MC-1. Appl ied Environ mental Microbiol ogy, 75(14): 4835–4852, https://doi.org/10.1128/AEM.02874-08.
Simmons S L, Sievert S M, Frankel R B, Bazylinski D A, Edwards K J. 2004. Spatiotemporal distribution of marine magnetotactic bacteria in a seasonally stratified coastal salt pond. Appl ied and Environ mental Microbiol ogy, 70(10): 6230–6239, https://doi.org/10.1128/AEM.70.10.6230-6239.2004.
Touchon M, Bernheim A, Rocha E P C. 2016. Genetic and lifehistory traits associated with the distribution of prophages in bacteria. The ISME Journal, 10(11): 2744–2754, https://doi.org/10.1038/ismej.2016.47.
Touchon M, de Sousa J A M, Rocha E P C. 2017. Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer. Current Opinion in Microbiology, 38: 66–73, https://doi.org/10.1016/j.mib.2017.04.010.
Trubitsyn D, Monteil C L, Geurink C, Morillo-Lopez V, de Almeida L G P, de Vasconcelos T R, Abreu F, Bazylinski D A, Lefevre C T. 2021. Complete genome sequence of strain SS-5, a magnetotactic gammaproteobacterium isolated from the Salton Sea, a Shallow, Saline, Endorheic Rift Lake located on the San Andreas Fault in California. Microbiology Resource Announcements, 10 (1): e00928–20, https://doi.org/10.1128/MRA.00928-20.
Uebe R, Schüler D, Jogler C, Wiegand S. 2018. Reevaluation of the complete genome sequence of Magnetospirillum gryphiswaldense MSR-1 with single-molecule real-time sequencing data. Genome Announcements, 6 (17): e00309–18, https://doi.org/10.1128/genomeA.00309-18.
Uzun M, Alekseeva L, Krutkina M, Koziaeva V, Grouzdev D. 2020. Unravelling the diversity of magnetotactic bacteria through analysis of open genomic databases. Scientific Data, 7(1): 252, https://doi.org/10.1038/s41597-020-00593-0.
Vali H, Förster O, Amarantidis G, Petersen N. 1987. Magnetotactic bacteria and their magnetofossils in sediments. Earth and Planetary Science Letters, 86(2—4): 389–400, https://doi.org/10.1016/0012-821X(87)90235-4.
Vallenet D, Belda E, Calteau A, Cruveiller S, Engelen S, Lajus A, Le Fèvre F, Longin C, Mornico D, Roche D, Rouy Z, Salvignol G, Scarpelli S, Smith A A T, Weiman M, Médigue C. 2013. MicroScope—an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Research, 41(D1): D636–D647, https://doi.org/10.1093/nar/gks1194.
Verschueren K H G, Franken S M, Rozeboom H J, Kalk K H, Dijkstra B W. 1993. Refined X-ray structures of haloalkane dehalogenase at pH 6.2 and pH 8.2 and implications for the reaction mechanism. Journal of Molecular Biology, 232(3): 856–872, https://doi.org/10.1006/jmbi.1993.1436.
Wang Y Z, Zhang T W, Lin W, Zhang B F, Cai Y, Yang C Y, Li J H, Xu H T, Pan Y X. 2016. Complete genome sequence of Magnetospirillum sp. strain XM-1, isolated from the Xi’an City moat, China. Genome Announcements, 4(5): e01171–16, https://doi.org/10.1128/genomeA.01171-16.
Wenter R, Wanner G, Schüler D, Overmann J. 2009. Ultrastructure, tactic behaviour and potential for sulfate reduction of a novel multicellular magnetotactic prokaryote from North Sea sediments. Environ mental Microbiol ogy, 11(6): 1493–1505, https://doi.org/10.1111/j.1462-2920.2009.01877.x.
Williams T J, Lefèvre C T, Zhao W D, Beveridge T J, Bazylinski D A. 2012. Magnetospira thiophila gen. nov., sp. nov., a marine magnetotactic bacterium that represents a novel lineage within the Rhodospirillaceae(Alphaproteobacteria). International Journal of Systematic and Evolutionary Microbiology, 62(Pt 10): 2443–2450, https://doi.org/10.1099/ijs.0.037697-0.
Yang C D, Takeyama H, Tanaka T, Matsunaga T. 2001. Effects of growth medium composition, iron sources and atmospheric oxygen concentrations on production of luciferase-bacterial magnetic particle complex by a recombinant Magnetospirillum magneticum AMB-1. Enzyme and Microbial Technology, 29(1): 13–19, https://doi.org/10.1016/S0141-0229(01)00343-X.
Zhou K, Zhang W Y, Pan H M, Li J H, Yue H D, Xiao T, Wu L F. 2013. Adaptation of spherical multicellular magnetotactic prokaryotes to the geochemically variable habitat of an intertidal zone. Environ mental Microbiol ogy, 15(5): 1595–1605, https://doi.org/10.1111/1462-2920.12057.
Zhu K L, Pan H M, Li J H, Yu-Zhang K, Zhang S D, Zhang W Y, Zhou K, Yue H D, Pan Y X, Xiao T, Wu L F. 2010. Isolation and characterization of a marine magnetotactic spirillum axenic culture QH-2 from an intertidal zone of the China Sea. Research in Microbiology, 161(4): 276–283, https://doi.org/10.1016/j.resmic.2010.02.003.
Acknowledgment
We thank Jianhong XU from Institute of Oceanology, Chinese Academy of Sciences and Weijia ZHANG from Institute of Deep-sea Science and Engineering, Chinese Academy of Sciences, for assistance in sampling.
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Supported by the National Natural Science Foundation of China—Shandong Joint Fund(No. U1706208) and the National Natural Science Foundation of China(Nos. 41776131, 41776130)
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Du, H., Zhang, W., Lin, W. et al. Genomic analysis of a pure culture of magnetotactic bacterium Terasakiella sp. SH-1. J. Ocean. Limnol. 39, 2097–2106 (2021). https://doi.org/10.1007/s00343-021-1054-5
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DOI: https://doi.org/10.1007/s00343-021-1054-5