Using magnetic nanoparticles to explore symbiotic interactions – Scientific Reports

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  • Munzi, S., Cruz, C. & Correa, A. When the exception becomes the rule: An integrative approach to symbiosis. Sci. Total Environ. 672, 855–861 (2019).


    Google Scholar
     

  • McFall-Ngai, M. Symbiosis takes a front and center role in biology. PLoS Biol. 22, e3002571 (2024).


    Google Scholar
     

  • Margulis, L. & Fester, R. Symbiosis as a source of evolutionary innovation: speciation and morphogenesis (MIT Press, 1991).

  • Maher, R. L. et al. Coral microbiomes demonstrate flexibility and resiliance through a reduction in community diversity following a thermal stress event. Front. Ecol. Evol. 14, 555698 (2020).


    Google Scholar
     

  • McFall-Ngai, M. Divining the essence of symbiosis: insights from the squid-vibrio model. PLoS Biol. 12, e1001783 (2014).


    Google Scholar
     

  • Perreau, J. & Moran, N. A. Genetic innovations in animal-microbe symbioses. Nat. Rev. Genet. 23, 23–39 (2022).


    Google Scholar
     

  • Engelberts, J. P., Robbins, S. J., D’amjanovic, K. & Webster, N. S. Integrating novel tools to elucidate the metabolic basis of microbial symbiosis in reef holobionts. Mar. Biol. 168, 175 (2021).


    Google Scholar
     

  • Jain, D., Jones, L. & Roy, S. Gene editing to improve legume-rhizobia symbiosis in a changing climate. Curr. Opin. Plant. Biol. 71, 102324 (2023).


    Google Scholar
     

  • Krishnan, K. M. Biomedical nanomagnetics: a spin through possibilities in imaging, diagnostics, and therapy. IEEE Trans. Magn. 46, 2523–2558 (2010).


    Google Scholar
     

  • Kianfar, E. Magnetic nanoparticles in targeted drug delivery: a review. J. Supercond Nov Magn. 34, 1709–1735 (2021).


    Google Scholar
     

  • Tay, Z. W. et al. Magnetic particle imaging-guided heating in vivo using gradient fields for arbitrary localization of magnetic hyperthermia therapy. ACS nano. 12, 3699–3713 (2018).


    Google Scholar
     

  • Fuller, E. G. et al. Theranostic nanocarriers combining high drug loading and magnetic particle imaging. Int. J. Pharm. 572, 118796 (2019).


    Google Scholar
     

  • Stueber, D. D., Villanova, J., Aponte, I., Xiao, Z. & Colvin, V. L. Magnetic nanoparticles in biology and medicine: past, present, and future trends. Pharmaceutics 13 (2021).

  • Liu, S. et al. Long circulating tracer tailored for magnetic particle imaging. Nanotheranostics 5, 348–361 (2021).


    Google Scholar
     

  • Mittal, A., Roy, I. & Gandhi, S. Magnetic nanoparticles: an overview for biomedical applications. Magnetochemistry 8, 107 (2022).


    Google Scholar
     

  • Stiufiuc, G. F. & Stiufiuc, R. I. Magnetic nanoparticles: synthesis, characterization, and their use in the biomedical field. Appl. Sci. 14, 1623 (2024).


    Google Scholar
     

  • Baki, A., Wiekhorst, F. & Bleul, R. Advances in magnetic nanoparticles engineering for biomedical applications: A review. Bioengineering (Basel) 8 (2021).

  • Nyholm, S. V. & McFall-Ngai, M. J. A lasting symbiosis: how the Hawaiian bobtail squid finds and keeps its bioluminescent bacterial partner. Nat. Rev. Microbiol. 19, 666–679 (2021).


    Google Scholar
     

  • Visick, K. L., Stabb, E. V. & Ruby, E. G. A lasting symbiosis: how Vibrio fischeri finds a squid partner and persists within its natural host. Nat. Rev. Microbiol. 19, 654–665 (2021).


    Google Scholar
     

  • McFall-Ngai, M. J. & Ruby, E. G. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 254, 1491–1494 (1991).


    Google Scholar
     

  • Imes, A. M. et al. Euprymna berryi as a comparative model host for Vibrio fischeri light organ symbiosis. Appl. Environ. Microbiol., e0000125 (2025).

  • McAnulty, S. J. & Nyholm, S. V. The role of hemocytes in the Hawaiian bobtail squid, Euprymna scolopes: a model organism for studying beneficial host-microbe interactions. Front. Microbiol. 7, 2013 (2016).


    Google Scholar
     

  • Koropatnick, T. A., Kimbell, J. R. & McFall-Ngai, M. J. Responses of host hemocytes during the initiation of the squid-vibrio symbiosis. Biol. Bull. 212, 29–39 (2007).


    Google Scholar
     

  • Rader, B., McAnulty, S., J, S. & Nyholm, V. Persistent symbiont colonization leads to a maturation of hemocyte response in the Euprymna scolopes/Vibrio fischeri symbiosis. MicrobiologyOpen 8, e858 (2019).


    Google Scholar
     

  • Schwartzman, J. A. et al. The chemistry of negotiation: rhythmic, glycan-driven acidification in a symbiotic conversation. Proc. Natl. Acad. Sci. USA 112, 566–571 (2015).

  • Tay, R. E. et al. High-efficiency magnetophoretic labelling of adoptively-transferred T cells for longitudinal in vivo magnetic particle imaging. Theranostics 14, 6138–6160 (2024).


    Google Scholar
     

  • Searle, B. C. Scaffold: a bioinformatic tool for validating MS/MS-based proteomic studies. Proteomics 10, 1265–1269 (2010).


    Google Scholar
     

  • Li, J. & Hu, Z. Research progress on damage-associated molecular patterns in acute kidney injury. Front. Immunol. 16, 1590822 (2025).


    Google Scholar
     

  • Richards, C. M., McRae, S. A., Ranger, A. L. & Klegeris, A. Extracellular histones as damage-associated molecular patterns in neuroinflammatory responses. Rev. Neurosci. 34, 533–558 (2023).


    Google Scholar
     

  • Schleicher, T. R., VerBerkmoes, N. C., Shah, M. & Nyholm, S. V. Colonization state influences the hemocyte proteome in a beneficial squid-Vibrio symbiosis. Mol. Cell. Proteom. 13, 2673–2686 (2014).


    Google Scholar
     

  • Longo, N., Frigeni, M. & Pasquali, M. Carnitine transport and fatty acid oxidation. Biochim. Biophys. Acta. 1863, 2422–2435 (2016).


    Google Scholar
     

  • Chen, X. et al. A non-invasive nanoparticles for multimodal imaging of ischemic myocardium in rats. J. Nanobiotechnol. 19, 82 (2021).


    Google Scholar
     

  • Rubio, J. M. et al. Group V secreted phospholipase A2 is upregulated by IL-4 in human macrophages and mediates phagocytosis via hydrolysis of ethanolamine phospholipids. J. Immunol. 194, 3327–3339 (2015).


    Google Scholar
     

  • Nyholm, S. V., Stewart, J. J. & Ruby, E. G. McFall-Ngai, M. J. Recognition between symbiotic Vibrio fischeri and the haemocytes of Euprymna scolopes. Environ. Microbiol. 11, 483–493 (2009).


    Google Scholar
     

  • Collins, A. J., Schleicher, T. R., Rader, B. A. & Nyholm, S. V. Understanding the role of host hemocytes in a squid/vibrio symbiosis using transcriptomics and proteomics. Front. Immunol. 3, 91 (2012).


    Google Scholar
     

  • Murphy, F. & Quinn, B. The effects of microplastic on freshwater Hydra attenuata feeding, morphology & reproduction. Environ. Pollut. 234, 487–494 (2018).


    Google Scholar
     

  • Jacobovitz, M. R. et al. Dinoflagellate symbionts escape vomocytosis by host cell immune suppression. Nat. Microbiol. 6, 769–782 (2021).


    Google Scholar
     

  • Marulanda-Gomez, A. M., Bayer, K., Pita, L. & Hentschel, U. A novel in-vivo phagocytosis assay to gain cellular insights on sponge-microbe interactions. Front. Mar. Sci. (2023).

  • Velazquez-Albino, A. C. & Imhoff, E. D. Rinaldi-Ramos, C. M. Advances in engineering nanoparticles for magnetic particle imaging (MPI). Sci. Adv. 11, eado7356 (2025).


    Google Scholar
     

  • Estelrich, J., Escribano, E., Queralt, J. & Busquets, M. A. Iron oxide nanoparticles for magnetically-guided and magnetically-responsive drug delivery. Int. J. Mol. Sci. 16, 8070–8101 (2015).


    Google Scholar
     

  • Zhao, Z., Torres-Díaz, I., Vélez, C., Arnold, D. P. & Rinaldi, C. Brownian dynamics simulations of magnetic nanoparticles captured in strong magnetic field gradients. J. Phys. Chem. C. 121, 801–810 (2016).


    Google Scholar
     

  • Bushra, R. et al. Recent advances in magnetic nanoparticles: key applications, environmental insights and future strategies. SM&T 40, e00985 (2024).

  • Pan, Y., Du, X., Zhao, F. & Xu, B. Magnetic nanoparticles for the manipulation of proteins and cells. Chem. Soc. Rev. 41, 2912–2942 (2012).


    Google Scholar
     

  • Zwi-Dantsis, L. et al. Remote Magnetic Nanoparticle Manipulation Enables the Dynamic Patterning of Cardiac Tissues. Adv. Mater. 32, e1904598 (2020).


    Google Scholar
     

  • Al-Obaidy, R., Haider, A. J., Al-Musawi, S. & Arsad, N. Targeted delivery of paclitaxel drug using polymer-coated magnetic nanoparticles for fibrosarcoma therapy: in vitro and in vivo studies. Sci. Rep. 13, 3180 (2023).


    Google Scholar
     

  • He, N. et al. Nano pom-poms prepared exosomes enable highly specific cancer biomarker detection. Commun. Biol. 5, 660 (2022).


    Google Scholar
     

  • Chen, Y. & Hou, S. Recent progress in the effect of magnetic iron oxide nanoparticles on cells and extracellular vesicles. Cell. Death Discov. 9, 195 (2023).


    Google Scholar
     

  • Unni, M. et al. Thermal decomposition synthesis of iron oxide nanoparticles with diminished magnetic dead layer by controlled addition of oxygen. ACS nano. 11, 2284–2303 (2017).


    Google Scholar
     

  • Butler-Struben, H. M., Brophy, S. M., Johnson, N. A. & Crook, R. J. vivo recording of neural and behavioral correlates of anesthesia induction, reversal, and euthanasia in cephalopod molluscs. Front. Physiol. 9, 109 (2018).


    Google Scholar
     

  • Fiorito, G. et al. Guidelines for the care and welfare of cephalopods in research -a consensus based on an initiative by CephRes, FELASA and the Boyd Group. Lab. Anim. 49, 1–90 (2015).


    Google Scholar
     

  • Collins, A. J. & Nyholm, S. V. Obtaining hemocytes from the Hawaiian bobtail squid Euprymna scolopes and observing their adherence to symbiotic and non-symbiotic bacteria. J. Vis. Exp. (2010).

  • Koch, E. et al. (ed, J.) The cytokine MIF controls daily rhythms of symbiont nutrition in an animal-bacterial association. Proc. Natl. Acad. Sci. USA 117 27578–27586 (2020).


    Google Scholar
     

  • Boettcher, K. J. & Ruby, E. G. Depressed light emission by symbiotic Vibrio fischeri of the sepiolid squid Euprymna scolopes. J. Bacteriol. 172, 3701–3706 (1990).


    Google Scholar
     

  • Koch, E. J. & Foster, J. S. Labeling of host immune cells with magnetic nanoparticles (protocols.io, 2024).

  • Cox, J. & Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367–1372 (2008).


    Google Scholar
     

  • Belcaid, M. et al. Symbiotic organs shaped by distinct modes of genome evolution in cephalopods. Proc. Natl. Acad. Sci. USA. 116, 3030–3035 (2019).


    Google Scholar
     

  • Tsugawa, H. et al. MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat. Methods. 12, 523–526 (2015).


    Google Scholar
     

  • NIST23. NIST23: updates of the NIST tandem and electron ionization spectral libraries (2023). https://www.nist.gov/programs-projects/nist23-updates-nist-tandem-and-electron-ionization-spectral-libraries

  • Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).


    Google Scholar
     

  • Team, R. C. R: A language and environment for statistical computing (2013). http://www.R-project.org/

  • Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multple testing. J. R. Stat. Soc. B 289–300 (1995).

  • Ward, J. H. Jr & Hook, M. E. Application of an hiercrchical grouping procedure to a problem of grouping profiles. Educ. Psychol. Meas. 23, 69–81 (1963).


    Google Scholar
     

  • Chen, H. & Boutros, P. C. VennDiagram: a package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinform. 12, 35 (2011).


    Google Scholar
     

  • Conway, J. R., Lex, A. & Gehlenborg, N. UpSetR: an R package for the visualization of intersecting sets and their properties. Bioinformatics 33, 2938–2940 (2017).


    Google Scholar
     

  • Good, H. J. et al. On the partial volume effect in magnetic particle imaging. Phys. Med. Biol. 70 (2025).

  • Kerwin, A. H., McAnulty, S. J. & Nyholm, S. V. Development of the accessory nidamental gland and associated bacterial community in the Hawaiian bobtail squid, Euprymna scolopes. Biol. Bull. 240, 205–218 (2021).


    Google Scholar