Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability

© 2018 American Chemical Society. In recent decades, biologists have sought to tag animals with various sensors to study aspects of their behavior otherwise inaccessible from controlled laboratory experiments. Despite this, chemical information, both environmental and physiological, remains challeng...

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Main Authors: Lee, Michael A, Nguyen, Freddy T, Scott, Kathleen, Chan, Nathan YL, Bakh, Naveed Ali, Jones, Kelvin K, Pham, Crystal, Garcia-Salinas, Pablo, Garcia-Parraga, Daniel, Fahlman, Andreas, Marco, Vicente, Koman, Volodymyr B, Oliver, Ronald J, Hopkins, Lloyd W, Rubio, Consuelo, Wilson, Rory P, Meekan, Mark G, Duarte, Carlos M, Strano, Michael S
Other Authors: Massachusetts Institute of Technology. Department of Chemical Engineering
Format: Article
Language:English
Published: American Chemical Society (ACS) 2021
Online Access:https://hdl.handle.net/1721.1/134899
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author Lee, Michael A
Nguyen, Freddy T
Scott, Kathleen
Chan, Nathan YL
Bakh, Naveed Ali
Jones, Kelvin K
Pham, Crystal
Garcia-Salinas, Pablo
Garcia-Parraga, Daniel
Fahlman, Andreas
Marco, Vicente
Koman, Volodymyr B
Oliver, Ronald J
Hopkins, Lloyd W
Rubio, Consuelo
Wilson, Rory P
Meekan, Mark G
Duarte, Carlos M
Strano, Michael S
author2 Massachusetts Institute of Technology. Department of Chemical Engineering
author_facet Massachusetts Institute of Technology. Department of Chemical Engineering
Lee, Michael A
Nguyen, Freddy T
Scott, Kathleen
Chan, Nathan YL
Bakh, Naveed Ali
Jones, Kelvin K
Pham, Crystal
Garcia-Salinas, Pablo
Garcia-Parraga, Daniel
Fahlman, Andreas
Marco, Vicente
Koman, Volodymyr B
Oliver, Ronald J
Hopkins, Lloyd W
Rubio, Consuelo
Wilson, Rory P
Meekan, Mark G
Duarte, Carlos M
Strano, Michael S
author_sort Lee, Michael A
collection MIT
description © 2018 American Chemical Society. In recent decades, biologists have sought to tag animals with various sensors to study aspects of their behavior otherwise inaccessible from controlled laboratory experiments. Despite this, chemical information, both environmental and physiological, remains challenging to collect despite its tremendous potential to elucidate a wide range of animal behaviors. In this work, we explore the design, feasibility, and data collection constraints of implantable, near-infrared fluorescent nanosensors based on DNA-wrapped single-wall carbon nanotubes (SWNT) embedded within a biocompatible poly(ethylene glycol) diacrylate (PEGDA) hydrogel. These sensors are enabled by Corona Phase Molecular Recognition (CoPhMoRe) to provide selective chemical detection for marine organism biologging. Riboflavin, a key nutrient in oxidative phosphorylation, is utilized as a model analyte in in vitro and ex vivo tissue measurements. Nine species of bony fish, sharks, eels, and turtles were utilized on site at Oceanogràfic in Valencia, Spain to investigate sensor design parameters, including implantation depth, sensor imaging and detection limits, fluence, and stability, as well as acute and long-term biocompatibility. Hydrogels were implanted subcutaneously and imaged using a customized, field-portable Raspberry Pi camera system. Hydrogels could be detected up to depths of 7 mm in the skin and muscle tissue of deceased teleost fish (Sparus aurata and Stenotomus chrysops) and a deceased catshark (Galeus melastomus). The effects of tissue heterogeneity on hydrogel delivery and fluorescence visibility were explored, with darker tissues masking hydrogel fluorescence. Hydrogels were implanted into a living eastern river cooter (Pseudemys concinna), a European eel (Anguilla anguilla), and a second species of catshark (Scyliorhinus stellaris). The animals displayed no observable changes in movement and feeding patterns. Imaging by high-resolution ultrasound indicated no changes in tissue structure in the eel and catshark. In the turtle, some tissue reaction was detected upon dissection and histopathology. Analysis of movement patterns in sarasa comet goldfish (Carassius auratus) indicated that the hydrogel implants did not affect swimming patterns. Taken together, these results indicate that this implantable form factor is a promising technique for biologging using aquatic vertebrates with further development. Future work will tune the sensor detection range to the physiological range of riboflavin, develop strategies to normalize sensor signal to account for the optical heterogeneity of animal tissues, and design a flexible, wearable device incorporating optoelectronic components that will enable sensor measurements in moving animals. This work advances the application of nanosensors to organisms beyond the commonly used rodent and zebrafish models and is an important step toward the physiological biologging of aquatic organisms.
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spelling mit-1721.1/1348992023-12-12T15:40:20Z Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability Lee, Michael A Nguyen, Freddy T Scott, Kathleen Chan, Nathan YL Bakh, Naveed Ali Jones, Kelvin K Pham, Crystal Garcia-Salinas, Pablo Garcia-Parraga, Daniel Fahlman, Andreas Marco, Vicente Koman, Volodymyr B Oliver, Ronald J Hopkins, Lloyd W Rubio, Consuelo Wilson, Rory P Meekan, Mark G Duarte, Carlos M Strano, Michael S Massachusetts Institute of Technology. Department of Chemical Engineering Massachusetts Institute of Technology. Division of Comparative Medicine © 2018 American Chemical Society. In recent decades, biologists have sought to tag animals with various sensors to study aspects of their behavior otherwise inaccessible from controlled laboratory experiments. Despite this, chemical information, both environmental and physiological, remains challenging to collect despite its tremendous potential to elucidate a wide range of animal behaviors. In this work, we explore the design, feasibility, and data collection constraints of implantable, near-infrared fluorescent nanosensors based on DNA-wrapped single-wall carbon nanotubes (SWNT) embedded within a biocompatible poly(ethylene glycol) diacrylate (PEGDA) hydrogel. These sensors are enabled by Corona Phase Molecular Recognition (CoPhMoRe) to provide selective chemical detection for marine organism biologging. Riboflavin, a key nutrient in oxidative phosphorylation, is utilized as a model analyte in in vitro and ex vivo tissue measurements. Nine species of bony fish, sharks, eels, and turtles were utilized on site at Oceanogràfic in Valencia, Spain to investigate sensor design parameters, including implantation depth, sensor imaging and detection limits, fluence, and stability, as well as acute and long-term biocompatibility. Hydrogels were implanted subcutaneously and imaged using a customized, field-portable Raspberry Pi camera system. Hydrogels could be detected up to depths of 7 mm in the skin and muscle tissue of deceased teleost fish (Sparus aurata and Stenotomus chrysops) and a deceased catshark (Galeus melastomus). The effects of tissue heterogeneity on hydrogel delivery and fluorescence visibility were explored, with darker tissues masking hydrogel fluorescence. Hydrogels were implanted into a living eastern river cooter (Pseudemys concinna), a European eel (Anguilla anguilla), and a second species of catshark (Scyliorhinus stellaris). The animals displayed no observable changes in movement and feeding patterns. Imaging by high-resolution ultrasound indicated no changes in tissue structure in the eel and catshark. In the turtle, some tissue reaction was detected upon dissection and histopathology. Analysis of movement patterns in sarasa comet goldfish (Carassius auratus) indicated that the hydrogel implants did not affect swimming patterns. Taken together, these results indicate that this implantable form factor is a promising technique for biologging using aquatic vertebrates with further development. Future work will tune the sensor detection range to the physiological range of riboflavin, develop strategies to normalize sensor signal to account for the optical heterogeneity of animal tissues, and design a flexible, wearable device incorporating optoelectronic components that will enable sensor measurements in moving animals. This work advances the application of nanosensors to organisms beyond the commonly used rodent and zebrafish models and is an important step toward the physiological biologging of aquatic organisms. 2021-10-27T20:09:45Z 2021-10-27T20:09:45Z 2019 2019-09-13T13:09:47Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/134899 en 10.1021/ACSSENSORS.8B00538 ACS Sensors Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf American Chemical Society (ACS) Other repository
spellingShingle Lee, Michael A
Nguyen, Freddy T
Scott, Kathleen
Chan, Nathan YL
Bakh, Naveed Ali
Jones, Kelvin K
Pham, Crystal
Garcia-Salinas, Pablo
Garcia-Parraga, Daniel
Fahlman, Andreas
Marco, Vicente
Koman, Volodymyr B
Oliver, Ronald J
Hopkins, Lloyd W
Rubio, Consuelo
Wilson, Rory P
Meekan, Mark G
Duarte, Carlos M
Strano, Michael S
Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability
title Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability
title_full Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability
title_fullStr Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability
title_full_unstemmed Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability
title_short Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability
title_sort implanted nanosensors in marine organisms for physiological biologging design feasibility and species variability
url https://hdl.handle.net/1721.1/134899
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