EPI-Cuticle, an interdisciplinary team-project on the biomimetics of insect Cuticle: the case study of the hemipteran stylet — a chitin-protein polymeric assemblage and an articulated biosyringe & drilling micro-engine.

BGPI : équipe 2 : Interactions Virus Insecte Plante (VIP)International audienceAphids are insect from the order Hemiptera, characterized by very specialized mouthparts of the piercing-sucking type, primarily adapted to plant feeding. Together with whiteflies and scale insects, aphids further adapted to a parasitic lifestyle and adaption to feeding on plant phloem, the tissue specialized in sugar distribution to growing plant tissues. During the course of the adaptation, aphids developed their extraordinary stylet apparatus (a 4-pieced biological syringe made of cuticle, a chitin- protein polymeric assemblage) to be a precision articulated drilling micro-engine able to avoid plant-cell injury, and capable of adopting a complex non-linear trajectory to its target tissue in spite of its extremely simple (evolutionary conserved) drawing plan. Only equipped with micro-mechanical sensors in its external mandibular stylets, it is able to circulate high-sugar or protein fluids (phloem sap or saliva) within its two-channel high viscosity microfluidic device.Within a single biological object, the aphid stylet, we developed a biomimetic multidisplinary project named EP-Cuticle, involving the preceding disciplinary objects: i) polymer science involving mixed P+C (cuticular protein+chitin/chitosan) polymer assemblage, ii) solid and iii) fluid mechanics aiming at understanding biomaterial movements withing the biosyringe, as well as iv) one ongoing module on μmechanical sensing.Our first results involved the first and full-characterization of the protein complement of the aphid stylets, including a comprehensive new class of cuticular proteins without chitin-binding modules (1,2), functioning the essential assembly zone, which seems to be the playground of the autoassembling which improve the multi-scale understanding of insect cuticule biogenesis. We aim at mimicking the properties of insect a-chitin, of the morphogenetic power of the substrate epidermal cell (3), and the multiscale-structuring properties originating in more-or-less complex arrays of cuticular proteins . Applications go from increasing the biomedical properties of chitosan polymeric implant and pharma- delivery devices (4); in understanding the mechanical key-properties of the 200 MY-evolved aphid/hemipteran stylet to improve (cardiac) surgical probe design (5); as well as understanding the surface molecular properties exhibited by natural (cuticle) or artificial (various film designs) P+C polymers: mimicking such nanosurface interactions is important to mimic the microbe-interaction properties of natural insect skin/cuticules, that display both micro-physical (6) and micro-chemical (7) interactions with many micro-organisms, being plant viruses or bacterial pathogens .Keywords :Biomaterial; Chitosan; Polymer alloy; AFM; Aphid; Vector biology1 Guschinskaya, N. et al. Insect Mouthpart Transcriptome Unveils Extension of Cuticular Protein Repertoire and Complex Organization. iScience 23, 100828, doi:10.1016/j.isci.2020.100828 (2020).2 Deshoux, M. et al. Cuticular Structure Proteomics in the Pea Aphid Acyrthosiphon pisum Reveals New Plant Virus Receptor Candidates at the Tip of Maxillary Stylets. J Proteome Res 19, 1319-1337, doi:10.1021/acs.jproteome.9b00851 (2020).3 Sviben, S. et al. Epidermal Cell Surface Structure and Chitin-Protein Co-assembly Determine Fiber Architecture in the Locust Cuticle. ACS Appl Mater Interfaces 12, 25581-25590, doi:10.1021/acsami.0c04572 (2020).4 Treguier, J. et al. Chitosan Films for Microfluidic Studies of Single Bacteria and Perspectives for Antibiotic Susceptibility Testing. mBio 10, doi:10.1128/mBio.01375-19 (2019).5 Gindre, J. et al. Finite element simulation of the insertion of guidewires during an EVAR procedure: example of a complex patient case, a first step toward patient-specific parameterized models. Int J Numer Method Biomed Eng 31, e02716, doi:10.1002/cnm.2716 (2015).6 Bhadra, C. M. et al. Subtle Variations in Surface Properties of Black Silicon Surfaces Influence the Degree of Bactericidal Efficiency. Nanomicro Lett 10, 36, doi:10.1007/s40820-017-0186-9 (2018).7 Webster, C. G. et al. Identification of plant virus receptor candidates in the stylets of their aphid vectors. J Virol, doi:10.1128/JVI.00432-18 (2018)