Uncovering the chemistry behind inducible morphological defences in the crustacean Daphnia magna via micro-Raman spectroscopy
1.
Currey, J. D. The failure of exoskeletons and endoskeletons. J. Morphol. 123, 1–16 (1967).
CAS PubMed Article PubMed Central Google Scholar
2.
Taylor, D. & Dirks, J.-H. Shape optimization in exoskeletons and endoskeletons: a biomechanics analysis. J. R. Soc. Interface 9, 3480–3489 (2012).
PubMed PubMed Central Article Google Scholar
3.
Boßelmann, F., Romano, P., Fabritius, H., Raabe, D. & Epple, M. The composition of the exoskeleton of two crustacea: The American lobster Homarusamericanus and the edible crab Cancerpagurus. Thermochim. Acta 463, 65–68 (2007).
Article CAS Google Scholar
4.
Tynyakov, J. et al. A crayfish molar tooth protein with putative mineralized exoskeletal chitinous matrix properties. J. Exp. Biol. 218, 3487–3498 (2015).
PubMed Article PubMed Central Google Scholar
5.
Sugawara, A. et al. Self-organization of oriented calcium carbonate/polymer composites: Effects of a matrix peptide isolated from the exoskeleton of a crayfish. Angew. Chemie – Int. Ed. 45, 2876–2879 (2006).
CAS Article Google Scholar
6.
Inoue, H., Ozaki, N. & Nagasawa, H. Purification and structural determination of a phosphorylated peptide with anti-calcification and chitin-binding activities in the exoskeleton of the crayfish, Procambarus clarkii. Biosci. Biotechnol. Biochem. 65, 1840–1848 (2001).
CAS PubMed Article PubMed Central Google Scholar
7.
Taylor, J. R. A., Hebrank, J. & Kier, W. M. Mechanical properties of the rigid and hydrostatic skeletons of molting blue crabs, Callinectes sapidus Rathbun. J. Exp. Biol. 210, 4272–4278 (2007).
PubMed Article PubMed Central Google Scholar
8.
Chen, P. Y., Lin, A. Y. M., McKittrick, J. & Meyers, M. A. Structure and mechanical properties of crab exoskeletons. Acta Biomater. 4, 587–596 (2008).
PubMed Article PubMed Central Google Scholar
9.
Cribb, B. W. et al. Structure, composition and properties of naturally occuring non-calcified crustacean cuticle. Arthropod Struct. Dev. 38, 173–178 (2009).
CAS PubMed Article Google Scholar
10.
Bentov, S., Weil, S., Glazer, L., Sagi, A. & Berman, A. Stabilization of amorphous calcium carbonate by phosphate rich organic matrix proteins and by single phosphoamino acids. J. Struct. Biol. 171, 207–215 (2010).
CAS PubMed Article PubMed Central Google Scholar
11.
Halcrow, K. Cell and tissue the fine structure of the carapace integument of Daphniamagna Straus (Crustacea Branchiopoda). Cell Tissue Res. 276, 267–276 (1976).
Google Scholar
12.
Benzie, J. A. H. Cladocera: The Genus Daphnia (Including Daphniopsis) Benzie Teil 1. Guides to the Identification of the Microinvertebrates of the Continental Waters of the World Vol. 21 (2005).
13.
Harvell, C. D. & Tollrian, R. The Ecology and Evolution of Inducible Defenses Vol. 65. (Princeton University Press, Princeton, 1999).
14.
Laforsch, C., Beccara, L. & Tollrian, R. Inducible defenses The relevance of chemical alarm cues in Daphnia. Limnol. Oceanogr. 51, 1466–1472 (2006).
ADS Article Google Scholar
15.
Tollrian, R. Predator-induced morphological defenses: Costs, life history shifts, and maternal effects in Daphniapulex. Ecology 76, 1691–1705 (1995).
Article Google Scholar
16.
Van Der Stap, I., Vos, M. & Mooij, W. M. Inducible defenses and rotifer food chain dynamics. Hydrobiologia 593, 103–110 (2007).
Article CAS Google Scholar
17.
Altwegg, R., Marchinko, K. B., Duquette, S. L. & Anholt, B. R. Dynamics of an inducible defence in the protist Euplotes. Arch. Hydrobiol. 160, 431–446 (2004).
Article Google Scholar
18.
Frost, S. D. W. The immune system as an inducible defense. in The Ecology and Evolution of Inducible Defenses 104–126 (1999).
19.
Grant, J. W. G. W. G. & Bayly, I. A. E. Predator induction of crests in morphs of the Daphnia carinata King complex. Limnol. Oceanogr. 26, 201–218 (1981).
20.
Laforsch, C. & Tollrian, R. Inducible defenses in multipredator environments: Cyclomorphosis in Daphniacucullata. Ecology 85, 2302–2311 (2004).
Article Google Scholar
21.
Ritschar, S., Rabus, M. & Laforsch, C. Predator-specific inducible morphological defenses of a water flea against two freshwater predators. J. Morphol. 281, 653–661 (2020).
PubMed Article Google Scholar
22.
Laforsch, C., Ngwa, W., Grill, W. & Tollrian, R. An acoustic microscopy technique reveals hidden morphological defenses in Daphnia. PNAS 101, 15911–15914 (2004).
ADS CAS PubMed Article Google Scholar
23.
Rabus, M., Söllradl, T., Clausen-Schaumann, H. & Laforsch, C. Uncovering ultrastructural defences in Daphniamagna. PLoS ONE 8, e67856 (2013).
ADS CAS PubMed PubMed Central Article Google Scholar
24.
Otte, K. A., Fröhlich, T., Arnold, G. J. & Laforsch, C. Proteomic analysis of Daphniamagna hints at molecular pathways involved in defensive plastic responses. BMC Genomics 15, 306 (2014).
PubMed PubMed Central Article CAS Google Scholar
25.
Otte, K. A., Schrank, I., Fröhlich, T., Arnold, G. J. & Laforsch, C. Interclonal proteomic responses to predator exposure in Daphnia magna may depend on predator composition of habitats. Mol. Ecol. 24, 3901–3917 (2015).
26.
Krafft, C. et al. Label-free molecular imaging of biological cells and tissues by linear and nonlinear Raman spectroscopic approaches. Angew. Chem. Int. Ed. 56, 4392–4430 (2017).
CAS Article Google Scholar
27.
Butler, H. J. et al. Using Raman spectroscopy to characterize biological materials. Nat. Protoc. 11, 664–687 (2016).
CAS PubMed Article PubMed Central Google Scholar
28.
Kuhar, N., Sil, S., Verma, T. & Umapathy, S. Challenges in application of Raman spectroscopy to biology and materials. RSC Adv. 8, 25888–25908 (2018).
CAS Article Google Scholar
29.
Talari, A. C. S., Movasaghi, Z., Rehman, S. & Rehman, I. U. Raman spectroscopy of biological tissues. Appl. Spectrosc. Rev. 50, 46–111 (2015).
ADS CAS Article Google Scholar
30.
Kruppert, S. et al. Push or Pull? The light-weight architecture of the Daphniapulex carapace is adapted to withstand tension, not compression. J. Morphol. 277, 1320–1328 (2016).
PubMed Article PubMed Central Google Scholar
31.
Gierlinger, N., Reisecker, C., Hild, S. & Gamsjaeger, S. Raman microscopy: Insights into chemistry and structure of biological materials. in Materials Design Inspired by Nature: Function Through Inner Architecture. 151–179 (2013). https://doi.org/10.1039/9781849737555-00151.
32.
Rabus, M., Waterkeyn, A., Van Pottelbergh, N., Brendonck, L. & Laforsch, C. Interclonal variation, effectiveness and long-term implications of Triops-induced morphological defences in Daphniamagna Strauss. J. Plankton Res. 34, 152–160 (2012).
Article Google Scholar
33.
Rabus, M. & Laforsch, C. Growing large and bulky in the presence of the enemy. Funct. Ecol. 25, 1137–1143 (2011).
Article Google Scholar
34.
Nikolov, S. et al. Robustness and optimal use of design principles of arthropod exoskeletons studied by ab initio-based multiscale simulations. J. Mech. Behav. Biomed. Mater. 4, 129–145 (2011).
CAS PubMed Article PubMed Central Google Scholar
35.
Al-Sawalmih, A., Li, C., Siegel, S., Fratzl, P. & Paris, O. On the stability of amorphous minerals in lobster cuticle. Adv. Mater. 21, 4011–4015 (2009).
CAS Article Google Scholar
36.
Luquet, G. Biomineralizations: Insights and prospects from crustaceans. Zookeys 176, 103–121 (2012).
Article Google Scholar
37.
Becker, A., Ziegler, A. & Epple, M. The mineral phase in the cuticles of two species of crustacea consists of magnesium calcite, amorphous calcium carbonate and amorphous calcium phosphate. R. Soc. Chem. 1814–1820 (2005).
38.
Roer, R. & Dillaman, R. The structure and clacification of the crustacean cuticle. Am. Zool. 24, 893–909 (1984).
CAS Article Google Scholar
39.
Gower, L. B. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem. Rev. 108, 4551–4627 (2008).
CAS PubMed Article Google Scholar
40.
Bots, P., Benning, L. G., Rodriguez-Blanco, J.-D., Roncal-Herrero, T. & Shaw, S. Mechanistic insights into the crystallization of amorphous calcium carbonate (ACC). Cryst. Growth Des. 12, 3806–3814 (2012).
CAS Article Google Scholar
41.
Addadi, L., Raz, S. & Weiner, S. Taking advantage of disorder: Amorphous calcium carbonate and its roles in biomineralization. Adv. Mater. 15, 959–970 (2003).
CAS Article Google Scholar
42.
Kawasaki, T. et al. Crystalline calcium phosphate and magnetic mineral content of Daphnia resting eggs. Zool. Sci. 21, 63–67 (2004).
CAS Article Google Scholar
43.
Gerrish, G. A. & Cáceres, C. E. Genetic versus environmental influence on pigment variation in the ephippia of Daphniapulicaria. Freshw. Biol. 48, 1971–1982 (2003).
Article Google Scholar
44.
Bentov, S., Abehsera, S. & Sagi, A. The mineralized exoskeletons of crustaceans. in (Cohen, E., Moussian, B. eds) Extracellular Composite Matrices in Arthropods 137–163. (Springer, Cham, 2016). https://doi.org/10.1007/978-3-319-40740-1.
45.
Weiner, S., Levi-Kalisman, Y., Raz, S. & Addadi, L. Biologically formed amorphous calcium carbonate. Connect. Tissue Res. 44, 214–218 (2003).
CAS PubMed Article Google Scholar
46.
Hessen, D. A. G. O. & Rukke, N. A. The costs of moulting in Daphnia; mineral regulation of carbon budgets. Freshw. Biol. 1, 169–178 (2000).
Article Google Scholar
47.
Waervagen, S. B., Rukke, N. A. & Hessen, D. O. Calcium content of crustacean zooplankton and its potential role in species distribution. Freshw. Biol. 47, 1866–1878 (2002).
CAS Article Google Scholar
48.
Nikolov, S. et al. Revealing the design principles of high-performance biological composites using Ab initio and multiscale simulations: The example of lobster cuticle. Adv. Mater. 22, 519–526 (2010).
CAS PubMed Article Google Scholar
49.
Bentov, S., Aflalo, E. D., Tynyakov, J., Glazer, L. & Sagi, A. Calcium phosphate mineralization is widely applied in crustacean mandibles. Sci. Rep. 6, 1–10 (2016).
Article CAS Google Scholar
50.
Raabe, D., Al-Sawalmih, A., Yi, S. B. & Fabritius, H. Preferred crystallographic texture of α-chitin as a microscopic and macroscopic design principle of the exoskeleton of the lobster Homarus americanus. Acta Biomater. 3, 882–895 (2007).
CAS PubMed Article PubMed Central Google Scholar
51.
Raabe, D. et al. Discovery of a honeycomb structure in the twisted plywood patterns of fibrous biological nanocomposite tissue. J. Cryst. Growth 283, 1–7 (2005).
ADS CAS Article Google Scholar
52.
Kruppert, S. et al. Biomechanical properties of predator-induced body armour in the freshwater crustacean Daphnia. Sci. Rep. 7, 1–13 (2017).
Article Google Scholar
53.
Azan, S. S. E. & Arnott, S. E. The impact of calcium decline on population growth rates of crustacean zooplankton in Canadian Shield lakes. Limnol. Oceanogr. 602–616 (2017). https://doi.org/10.1002/lno.10653.
54.
Riessen, H. P. et al. Changes in water chemistry can disable plankton prey defenses. Proc. Natl. Acad. Sci. U. S. A. 109, 15377–15382 (2012).
ADS CAS PubMed PubMed Central Article Google Scholar
55.
Tan, Q.-G. & Wang, W.-X. The regulation of calcium in Daphniamagna reared in different calcium environments. Limnol. Oceanogr. 54, 746–756 (2009).
ADS CAS Article Google Scholar
56.
Elendt, B. P. Selenium deficiency in Crustacea. Protoplasma 154, 25–33 (1990).
CAS Article Google Scholar
57.
Team, R. C. R: A Language and Environment for Statistical Computing. (2008).
58.
Ramoji, A. et al. Raman Spectroscopy follows time-dependent changes in T lymphocytes isolated from spleen of endotoxemic mice. ImmunoHorizons 3, 45–60 (2019).
CAS PubMed Article PubMed Central Google Scholar
59.
Chaturvedi, D. et al. Different phases of breast cancer cells: Raman study of immortalized, transformed, and invasive cells. Biosensors 6 (2016).
60.
Laforsch & Tollrian. A new preparation technique of daphnids for Scanning Electron Microscopy using hexamethyldisilazane. rch. Hydrobiol. 149, 587–596 (2000).
61.
Rohlf, F. J. & Sokal, R. R. Statistical tables. (1995). More