Mechanosensory Behaviour and Biotremology in Nematodes

Sugi, Takuma

doi:10.1007/978-3-030-97419-0_12

Mechanosensory Behaviour and Biotremology in Nematodes

Takuma Sugi⁸

Chapter
First Online: 25 May 2022

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Part of the Animal Signals and Communication book series (ANISIGCOM,volume 8)

Abstract

Nematodes account for approximately 80% of all animals on earth, which, inevitably, has diverse effects on ecosystems. Among diverse nematode species, Caenorhabditis elegans has been used as a powerful animal model through which to investigate mechanosensory behaviour and its underlying neural and molecular mechanisms. Furthermore, physical interactions between C. elegans and other nematode species and other animals, which have potentially become a good model for understanding biotremology, are discussed. In this chapter, I mainly review the mechanosensory behaviour of nematodes, especially C. elegans, and the perspectives on biotremology.

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References

Albeg A, Smith CJ, Chatzigeorgiou M, Feitelson DG, Hall DH, Schafer WR, Miller Iii DM, Treinin M (2011) C. elegans multi-dendritic sensory neurons: morphology and function. Mol Cell Neurosci 46:308–317. https://doi.org/10.1016/j.mcn.2010.10.001
CAS CrossRef PubMed Google Scholar
Altshuler DL, Dickson WB, Vance JT, Roberts SP, Dickinson MH (2005) Short-amplitude high-frequency wing strokes determine the aerodynamics of honeybee flight. Proc Natl Acad Sci USA 102:18213–18218. https://doi.org/10.1073/pnas.0506590102
CAS CrossRef PubMed PubMed Central Google Scholar
Arnadóttir J, O’Hagan R, Chen Y, Goodman MB, Chalfie M (2011) The DEG/ENaC protein MEC-10 regulates the transduction channel complex in Caenorhabditis elegans touch receptor neurons. J Neurosci 31:12695–12704. https://doi.org/10.1523/JNEUROSCI.4580-10.2011
CAS CrossRef PubMed PubMed Central Google Scholar
Bar-On YM, Phillips R, Milo R (2018) The biomass distribution on earth. Proc Natl Acad Sci USA 115:6506–6511. https://doi.org/10.1073/pnas.1711842115
CAS CrossRef PubMed PubMed Central Google Scholar
Barrière A, Félix M-A (2005) High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr Biol 15:1176–1184. https://doi.org/10.1016/j.cub.2005.06.022
CAS CrossRef PubMed Google Scholar
Bozorgmehr T, Ardiel EL, McEwan AH, Rankin CH (2013) Mechanisms of plasticity in a Caenorhabditis elegans mechanosensory circuit. Front Physiol 4:88. https://doi.org/10.3389/fphys.2013.00088
CrossRef PubMed PubMed Central Google Scholar
Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94
CAS CrossRef Google Scholar
Brownell PH (1977) Compressional and surface waves in sand used by desert scorpions to locate prey. Science 197:479–482
CAS CrossRef Google Scholar
Campbell JF, Gaugler R (1993) Nictation behaviour and its ecological implications in the host search strategies of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae). Behaviour 126:155–169. https://doi.org/10.1163/156853993x00092
CrossRef Google Scholar
Campbell JF, Kaya HK (1999) How and why a parasitic nematode jumps. Nature 397:485–486. https://doi.org/10.1038/17254
CAS CrossRef Google Scholar
Chalfie M, Au M (1989) Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243(4894):1027–1033
CAS CrossRef Google Scholar
Chalfie M, Sulston J (1981) Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol 82:358–370
CAS CrossRef Google Scholar
Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S (1985) The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5:956–964
CAS CrossRef Google Scholar
Chatzigeorgiou M, Schafer WR (2011) Lateral facilitation between primary mechanosensory neurons controls nose touch perception in C. elegans. Neuron 70:299–309. https://doi.org/10.1016/j.neuron.2011.02.046
CAS CrossRef PubMed PubMed Central Google Scholar
Chatzigeorgiou M, Yoo S, Watson JD, Lee W-H, Spencer WC, Kindt KS, Hwang SW, Miller DM, Treinin M, Driscoll M, Schafer WR (2010) Specific roles for DEG/ENaC and TRP channels in touch and thermosensation in C. elegans nociceptors. Nat Neurosci 13:861–868. https://doi.org/10.1038/nn.2581
CAS CrossRef PubMed PubMed Central Google Scholar
Chatzigeorgiou M, Bang S, Hwang SW, Schafer WR (2013) tmc-1 encodes a sodium-sensitive channel required for salt chemosensation in C. elegans. Nature 494:95–99. https://doi.org/10.1038/nature11845
CAS CrossRef PubMed PubMed Central Google Scholar
Chen X, Chalfie M (2014) Modulation of C. elegans touch sensitivity is integrated at multiple levels. J Neurosci 34:6522–6536. https://doi.org/10.1523/JNEUROSCI.0022-14.2014
CAS CrossRef PubMed Google Scholar
Chen Y, Bharill S, Isacoff EY, Chalfie M (2015) Subunit composition of a DEG/ENaC mechanosensory channel of Caenorhabditis elegans. Proc Natl Acad Sci USA 112:11690–11695. https://doi.org/10.1073/pnas.1515968112
CAS CrossRef PubMed PubMed Central Google Scholar
Coste B, Mathur J, Schmidt M, Earley TJ, Ranade S, Petrus MJ, Dubin AE, Patapoutian A (2010) Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330:55–60
CAS CrossRef Google Scholar
Cronin CJ, Mendel JE, Mukhtar S, Kim Y-M, Stirbl RC, Bruck J, Sternberg PW (2005) An automated system for measuring parameters of nematode sinusoidal movement. BMC Genet 6:5–19. https://doi.org/10.1186/1471-2156-6-5
CAS CrossRef PubMed PubMed Central Google Scholar
de Bono M, Bargmann CI (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94:679–689
CrossRef Google Scholar
de Bono M, Maricq AV (2005) Neuronal substrates of complex behaviors in C. elegans. Annu Rev Neurosci 28:451–501. https://doi.org/10.1146/annurev.neuro.27.070203.144259
CAS CrossRef PubMed Google Scholar
Ding SS, Schumacher LJ, Javer AE, Endres RG, Brown AE (2019) Shared behavioral mechanisms underlie C. elegans aggregation and swarming. eLife 8:1181. https://doi.org/10.7554/eLife.43318
CrossRef Google Scholar
Driscoll M, Chalfie M (1991) The mec-4 gene is a member of a family of Caenorhabditis elegans genes that can mutate to induce neuronal degeneration. Nature 349:588–593. https://doi.org/10.1038/349588a0
CAS CrossRef PubMed Google Scholar
Eastwood AL, Sanzeni A, Petzold BC, Park S-J, Vergassola M, Pruitt BL, Goodman MB (2015) Tissue mechanics govern the rapidly adapting and symmetrical response to touch. Proc Natl Acad Sci USA 112:E6955–E6963. https://doi.org/10.1073/pnas.1514138112
CAS CrossRef PubMed PubMed Central Google Scholar
Fang-Yen C, Wyart M, Xie J, Kawai R, Kodger T, Chen S, Wen Q, Samuel ADT (2010) Biomechanical analysis of gait adaptation in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 107:20323–20328. https://doi.org/10.1073/pnas.1003016107
CrossRef PubMed PubMed Central Google Scholar
Frézal L, Félix M-A (2015) C. elegans outside the Petri dish. eLife 4:381. https://doi.org/10.7554/eLife.05849
CrossRef Google Scholar
Fry SN, Sayaman R, Dickinson MH (2005) The aerodynamics of hovering flight in Drosophila. J Exp Biol 208:2303–2318. https://doi.org/10.1242/jeb.01612
CrossRef PubMed Google Scholar
Gannon TN, Rankin CH (1995) Methods of studying behavioral plasticity in Caenorhabditis elegans. Methods Cell Biol 48:205–223
CAS CrossRef Google Scholar
Geffeney SL, Goodman MB (2012) How we feel: ion channel partnerships that detect mechanical inputs and give rise to touch and pain perception. Neuron 74:609–619. https://doi.org/10.1016/j.neuron.2012.04.023
CAS CrossRef PubMed PubMed Central Google Scholar
Geffeney SL, Cueva JG, Glauser DA, Doll JC, Lee TH-C, Montoya M, Karania S, Garakani AM, Pruitt BL, Goodman MB (2011) DEG/ENaC but not TRP channels are the major mechanoelectrical transduction channels in a C. elegans nociceptor. Neuron 71:845–857. https://doi.org/10.1016/j.neuron.2011.06.038
CAS CrossRef PubMed PubMed Central Google Scholar
Goodman MB, Sengupta P (2019) How Caenorhabditis elegans senses mechanical stress, temperature, and other physical stimuli. Genetics 212:25–51. https://doi.org/10.1534/genetics.118.300241
CAS CrossRef PubMed PubMed Central Google Scholar
Hallem EA, Dillman AR, Hong AV, Zhang Y, Yano JM, DeMarco SF, Sternberg PW (2011) A sensory code for host seeking in parasitic nematodes. Curr Biol 21:377–383. https://doi.org/10.1016/j.cub.2011.01.048
CAS CrossRef PubMed PubMed Central Google Scholar
Hart AC, Sims S, Kaplan JM (1995) Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378:82–85. https://doi.org/10.1038/378082a0
CAS CrossRef PubMed Google Scholar
Hill PSM, Wessel A (2016) Primer: biotremology. Curr Biol 26:R187–R191
CAS CrossRef Google Scholar
Holbrook RI, Mortimer B (2018) Vibration sensitivity found in Caenorhabditis elegans. J Exp Biol 221. https://doi.org/10.1242/jeb.178947
Huang M, Chalfie M (1994) Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature 367:467–470. https://doi.org/10.1038/367467a0
CAS CrossRef PubMed Google Scholar
Kang L, Gao J, Schafer WR, Xie Z, Xu XZS (2010) C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron 67:381–391. https://doi.org/10.1016/j.neuron.2010.06.032
CAS CrossRef PubMed PubMed Central Google Scholar
Kim J, Kwon J-T, Kim H-S, Han J-H (2013) CREB and neuronal selection for memory trace. Front Neural Circuits 7:44. https://doi.org/10.3389/fncir.2013.00044
CrossRef PubMed PubMed Central Google Scholar
Kindt KS, Quast KB, Giles AC, De S, Hendrey D, Nicastro I, Rankin CH, Schafer WR (2007a) Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans. Neuron 55:662–676. https://doi.org/10.1016/j.neuron.2007.07.023
CAS CrossRef PubMed Google Scholar
Kindt KS, Viswanath V, Macpherson L, Quast K, Hu H, Patapoutian A, Schafer WR (2007b) Caenorhabditis elegans TRPA-1 functions in mechanosensation. Nat Neurosci 10:568–577. https://doi.org/10.1038/nn1886
CAS CrossRef PubMed Google Scholar
Kubanek J, Shukla P, Das A, Baccus SA, Goodman MB (2018) Ultrasound elicits behavioral responses through mechanical effects on neurons and ion channels in a simple nervous system. J Neurosci 38:3081–3091. https://doi.org/10.1523/JNEUROSCI.1458-17.2018
CAS CrossRef PubMed PubMed Central Google Scholar
Lee H, Choi M-K, Lee D, Kim H-S, Hwang H, Kim H, Park S, Paik Y-K, Lee J (2011) Nictation, a dispersal behavior of the nematode Caenorhabditis elegans, is regulated by IL2 neurons. Nat Neurosci. https://doi.org/10.1038/nn.2975
Leifer AM, Fang-Yen C, Gershow M, Alkema MJ, Samuel ADT (2011) Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nat Methods 8:147–152. https://doi.org/10.1038/nmeth.1554
CAS CrossRef PubMed PubMed Central Google Scholar
Li W, Feng Z, Sternberg PW, Xu XZS (2006) A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440:684–687. https://doi.org/10.1038/nature04538
CAS CrossRef PubMed PubMed Central Google Scholar
Li W, Kang L, Piggott BJ, Feng Z, Xu XZS (2011) The neural circuits and sensory channels mediating harsh touch sensation in Caenorhabditis elegans. Nat Commun 2:315. https://doi.org/10.1038/ncomms1308
CrossRef PubMed Google Scholar
Lonze BE, Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605–623
CAS CrossRef Google Scholar
Maguire SM, Clark CM, Nunnari J, Pirri JK, Alkema MJ (2011) The C. elegans touch response facilitates escape from predacious fungi. Curr Biol 21(15):P1326–P1330. https://doi.org/10.1016/j.cub.2011.06.063
CAS CrossRef Google Scholar
McClanahan PD, Xu JH, Fang-Yen C (2017) Comparing Caenorhabditis elegans gentle and harsh touch response behavior using a multiplexed hydraulic microfluidic device. Integr Biol (Camb) 82:1–10. https://doi.org/10.1039/C7IB00120G
CrossRef Google Scholar
Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10:3959–3970
CAS CrossRef Google Scholar
Mori I, Ohshima Y (1995) Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376:344–348. https://doi.org/10.1038/376344a0
CAS CrossRef PubMed Google Scholar
Mortimer B (2017) Biotremology: do physical constraints limit the propagation of vibrational information? Anim Behav 130:165–174
CrossRef Google Scholar
Nekimken AL, Fehlauer H, Kim AA, Manosalvas-Kjono SN, Ladpli P, Memon F, Gopisetty D, Sanchez V, Goodman MB, Pruitt BL, Krieg M (2017) Pneumatic stimulation of C. elegans mechanoreceptor neurons in a microfluidic trap. Lab Chip 17:1116–1127. https://doi.org/10.1039/C6LC01165A
CAS CrossRef PubMed PubMed Central Google Scholar
Nishida Y, Sugi T, Nonomura M, Mori I (2011) Identification of the AFD neuron as the site of action of the CREB protein in Caenorhabditis elegans thermotaxis. EMBO Rep 12:855–862. https://doi.org/10.1038/embor.2011.120
CAS CrossRef PubMed PubMed Central Google Scholar
O’Hagan R, Chalfie M, Goodman MB (2005) The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat Neurosci 8:43–50. https://doi.org/10.1038/nn1362
CAS CrossRef PubMed Google Scholar
Park S-J, Goodman MB, Pruitt BL (2007) Analysis of nematode mechanics by piezoresistive displacement clamp. Proc Natl Acad Sci USA 104:17376–17381. https://doi.org/10.1073/pnas.0702138104
CrossRef PubMed PubMed Central Google Scholar
Ranade SS, Syeda R, Patapoutian A (2015) Mechanically activated ion channels. Neuron 87:1162–1179. https://doi.org/10.1016/j.neuron.2015.08.032
CAS CrossRef PubMed PubMed Central Google Scholar
Rankin CH, Wicks SR (2000) Mutations of the Caenorhabditis elegans brain-specific inorganic phosphate transporter eat-4 affect habituation of the tap-withdrawal response without affecting the response itself. J Neurosci 20:4337–4344
CAS CrossRef Google Scholar
Reed EM, Wallace HR (1965) Leaping locomotion by an insect-parasitic nematode. Nature 206:210–211
CrossRef Google Scholar
Rose JK, Kaun KR, Chen SH, Rankin CH (2003) GLR-1, a non-NMDA glutamate receptor homolog, is critical for long-term memory in Caenorhabditis elegans. J Neurosci 23:9595–9599
CAS CrossRef Google Scholar
Sasakura H, Mori I (2013) Behavioral plasticity, learning, and memory in C. elegans. Curr Opin Neurobiol 23:92–99. https://doi.org/10.1016/j.conb.2012.09.005
CAS CrossRef PubMed Google Scholar
Schafer WR (2014) Mechanosensory molecules and circuits in C. elegans. Pflûgers Archiv Eur J Physiol 467:39–48. https://doi.org/10.1007/s00424-014-1574-3
CAS CrossRef Google Scholar
Schmid S, Wilson DA, Rankin CH (2014) Habituation mechanisms and their importance for cognitive function. Front Integr Neurosci 8:97. https://doi.org/10.3389/fnint.2014.00097
CrossRef PubMed Google Scholar
Stirman JN, Crane MM, Husson SJ, Wabnig S, Schultheis C, Gottschalk A, Lu H (2011) Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat Methods 8:153–158. https://doi.org/10.1038/nmeth.1555
CAS CrossRef PubMed PubMed Central Google Scholar
Sugi T, Nishida Y, Mori I (2011) Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat Neurosci 14:984–992. https://doi.org/10.1038/nn.2854
CAS CrossRef PubMed Google Scholar
Sugi T, Ohtani Y, Kumiya Y, Igarashi R, Shirakawa M (2014) High-throughput optical quantification of mechanosensory habituation reveals neurons encoding memory in Caenorhabditis elegans. Proc Natl Acad Sci USA 111:17236–17241. https://doi.org/10.1073/pnas.1414867111
CAS CrossRef PubMed PubMed Central Google Scholar
Sugi T, Okumura E, Kiso K, Igarashi R (2016) Nanoscale mechanical stimulation method for quantifying C. elegans mechanosensory behavior and memory. Ann Sci 32:1159–1164. https://doi.org/10.2116/analsci.32.1159
CAS CrossRef Google Scholar
Sugi T, Igarashi R, Nishimura M (2018) Noninvasive mechanochemical imaging in unconstrained Caenorhabditis elegans. Materials (Basel) 11(6):1034. https://doi.org/10.3390/ma11061034
CAS CrossRef Google Scholar
Sugi T, Ito H, Nishimura M, Nagai KH (2019) C. elegans collectively forms dynamical networks. Nat Commun 10:1–9. https://doi.org/10.1038/s41467-019-08537-y
CAS CrossRef Google Scholar
Suzuki H, Kerr R, Bianchi L, Frøkjaer-Jensen C, Slone D, Xue J, Gerstbrein B, Driscoll M, Schafer WR (2003) In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron 39:1005–1017
CAS CrossRef Google Scholar
Swierczek NA, Giles AC, Rankin CH, Kerr RA (2011) High-throughput behavioral analysis in C. elegans. Nat Methods 8:592–598. https://doi.org/10.1038/nmeth.1625
CAS CrossRef PubMed PubMed Central Google Scholar
Timbers TA, Rankin CH (2011) Tap withdrawal circuit interneurons require CREB for long-term habituation in Caenorhabditis elegans. Behav Neurosci 125:560–566. https://doi.org/10.1037/a0024370
CrossRef PubMed Google Scholar
White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B 314:1–340
CAS CrossRef Google Scholar
Wicks SR, Rankin CH (1995) Integration of mechanosensory stimuli in Caenorhabditis elegans. J Neurosci 15:2434–2444
CAS CrossRef Google Scholar
Yoshida K, Hirotsu T, Tagawa T, Oda S, Wakabayashi T, Iino Y, Ishihara T (2012) Odour concentration-dependent olfactory preference change in C. elegans. Nat Commun 3(739). https://doi.org/10.1038/ncomms1750
Zhou W, Wang J, Wang K, Huang B, Niu L, Li F, Cai F, Chen Y, Liu X, Zhang X, Cheng H, Kang L, Meng L, Zheng H (2017) Ultrasound neuro-modulation chip: activation of sensory neurons in Caenorhabditis elegans by surface acoustic waves. Lab Chip 17:1725–1731. https://doi.org/10.1039/C7LC00163K
CAS CrossRef PubMed Google Scholar

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Acknowledgements

This work was supported by JSPS KAKENHI Grant-in-Aid for Scientific Research (B) (grant number JP18H02483) and on Innovative areas “Science of Soft Robot” project (grant nmuber JP18H05474), by the PRESTO from Japan Science and Technology Agency (grant number JPMJPR12A9) and by the PRIME from Japan Agency for Medical Research and Development (grant number 19gm6110022h001).

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Program of Biomedical Science, Graduate School of Integrated Sciences for Life, Hiroshima University, Hiroshima, Japan
Takuma Sugi

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Correspondence to Takuma Sugi .

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Department of Biological Science, University of Tulsa, Tulsa, OK, USA
Dr. Peggy S. M. Hill
Research and Innovation Centre, Fondazione Edmund Mach, San Michele all’Adige, Trento, Italy
Valerio Mazzoni
Department of Organisms and Ecosystems Research, National Institute of Biology (NIB), Ljubljana, Slovenia
Nataša Stritih-Peljhan
Department of Organisms and Ecosystems Research, National Institute of Biology, Ljubljana, Slovenia
Meta Virant-Doberlet
Center for Integrative Biodiversity Discovery, Museum für Naturkunde - Leibniz Institute for Research on Evolution and Biodiversity, Berlin, Germany
Andreas Wessel

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Sugi, T. (2022). Mechanosensory Behaviour and Biotremology in Nematodes. In: Hill, P.S.M., Mazzoni, V., Stritih-Peljhan, N., Virant-Doberlet, M., Wessel, A. (eds) Biotremology: Physiology, Ecology, and Evolution. Animal Signals and Communication, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-030-97419-0_12

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DOI: https://doi.org/10.1007/978-3-030-97419-0_12
Published: 25 May 2022
Publisher Name: Springer, Cham
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Online ISBN: 978-3-030-97419-0
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