Tandem metabolic reaction–based sensors unlock in vivo metabolomics

X Xuanbing Cheng (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) Z Zongqi Li (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) J Jialun Zhu (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) J Jingyu Wang (Department of Engineering Science, University of Oxford) R Ruyi Huang (Department of Neurosurgery, David Geffen School of Medicine, University of California) L Lewis W. Yu (Department of Integrative Biology and Physiology, University of California) S Shuyu Lin (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) S Sarah Forman (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) E Evelina Gromilina (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) S Sameera Puri (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) P Pritesh Patel (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) M Mohammadreza Bahramian (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) J Jiawei Tan (State Key Laboratory of Chemical Biology, Shanghai Institute of Organic Chemistry, University of Chinese Academy of Sciences, Chinese Academy of Sciences, 345 Lingling Road, Shanghai 200032 China) H Hannaneh Hojaiji (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) D David Jelinek (Department of Molecular, Cell and Developmental Biology, University of California) L Laurent Voisin (Department of Molecular, Cell and Developmental Biology, University of California) K Kristie B. Yu (Department of Integrative Biology and Physiology, University of California) A Ao Zhang C Connie Ho (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California) L Lei Lei (Department of Molecular, Cell and Developmental Biology, University of California) H Hilary A. Coller (Department of Molecular, Cell and Developmental Biology, University of California) E Elaine Y. Hsiao (Department of Integrative Biology and Physiology, University of California) B Beck L. Reyes (Division of Pediatric Neurology, Department of Pediatrics, University of California) J Joyce H. Matsumoto (Division of Pediatric Neurology, Department of Pediatrics, University of California) D Daniel C. Lu (Department of Neurosurgery, David Geffen School of Medicine, University of California) C Chong Liu (Department of Chemistry and Biochemistry) C Carlos Milla (The Stanford Cystic Fibrosis Center, Center for Excellence in Pulmonary Biology, Stanford University School of Medicine) R Ronald W. Davis (Department of Biochemistry, School of Medicine, Stanford University) S Sam Emaminejad (Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California)

Abstract

Mimicking metabolic pathways on electrodes enables in vivo metabolite monitoring for decoding metabolism. Conventional in vivo sensors cannot accommodate underlying complex reactions involving multiple enzymes and cofactors, addressing only a fraction of enzymatic reactions for few metabolites. We devised a single-wall-carbon-nanotube-electrode architecture supporting tandem metabolic pathway–like reactions linkable to oxidoreductase-based electrochemical analysis, making a vast majority of metabolites detectable in vivo. This architecture robustly integrates cofactors, self-mediates reactions at maximum enzyme capacity, and facilitates metabolite intermediation/detection and interference inactivation through multifunctional enzymatic use. Accordingly, we developed sensors targeting 12 metabolites, with 100-fold-enhanced signal-to-noise ratio and days-long stability. Leveraging these sensors, we monitored trace endogenous metabolites in sweat/saliva for noninvasive health monitoring, and a bacterial metabolite in the brain, marking a key milestone for unraveling gut microbiota–brain axis dynamics.

Article Details

Volume / Issue Vol. 122, Issue 9
Published March 04, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (29)

X

Xuanbing Cheng

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

Z

Zongqi Li

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

J

Jialun Zhu

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

J

Jingyu Wang

Department of Engineering Science, University of Oxford

R

Ruyi Huang

Department of Neurosurgery, David Geffen School of Medicine, University of California

L

Lewis W. Yu

Department of Integrative Biology and Physiology, University of California

S

Shuyu Lin

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

S

Sarah Forman

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

E

Evelina Gromilina

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

S

Sameera Puri

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

P

Pritesh Patel

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

M

Mohammadreza Bahramian

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

J

Jiawei Tan

State Key Laboratory of Chemical Biology, Shanghai Institute of Organic Chemistry, University of Chinese Academy of Sciences, Chinese Academy of Sciences, 345 Lingling Road, Shanghai 200032 China

H

Hannaneh Hojaiji

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

D

David Jelinek

Department of Molecular, Cell and Developmental Biology, University of California

L

Laurent Voisin

Department of Molecular, Cell and Developmental Biology, University of California

K

Kristie B. Yu

Department of Integrative Biology and Physiology, University of California

A

Ao Zhang

C

Connie Ho

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California

L

Lei Lei

Department of Molecular, Cell and Developmental Biology, University of California

H

Hilary A. Coller

Department of Molecular, Cell and Developmental Biology, University of California

E

Elaine Y. Hsiao

Department of Integrative Biology and Physiology, University of California

B

Beck L. Reyes

Division of Pediatric Neurology, Department of Pediatrics, University of California

J

Joyce H. Matsumoto

Division of Pediatric Neurology, Department of Pediatrics, University of California

D

Daniel C. Lu

Department of Neurosurgery, David Geffen School of Medicine, University of California

C

Chong Liu

Department of Chemistry and Biochemistry

C

Carlos Milla

The Stanford Cystic Fibrosis Center, Center for Excellence in Pulmonary Biology, Stanford University School of Medicine

R

Ronald W. Davis

Department of Biochemistry, School of Medicine, Stanford University

S

Sam Emaminejad

Interconnected and Integrated Bioelectronics Lab (I²BL), Department of Electrical and Computer Engineering, Samueli School of Engineering, University of California