Engineering High-Yield Biopolymer Secretion Creates an Extracellular Protein Matrix for Living Materials

Orozco-Hidalgo, Maria Teresa; Charrier, Marimikel; Tjahjono, Nicholas; Tesoriero, Jr., Robert F.; Li, Dong; Molinari, Sara; Ryan, Kathleen R.; Ashby, Paul D.; Rad, Behzad; Ajo-Franklin, Caroline M.; Tullman-Ercek, ed., Danielle; Salmeron-Sanchez, Manuel

doi:10.1128/mSystems.00903-20

Title: Engineering High-Yield Biopolymer Secretion Creates an Extracellular Protein Matrix for Living Materials

Journal Article · Tue Apr 27 00:00:00 EDT 2021 · mSystems

DOI:https://doi.org/10.1128/mSystems.00903-20· OSTI ID:1772263

Orozco-Hidalgo, Maria Teresa ^[1];

^[1];

^[1]; Tesoriero, Jr., Robert F. ^[2]; Li, Dong ^[1]; Molinari, Sara ^[2];

^[3]; Ashby, Paul D. ^[1]; Rad, Behzad ^[1];

^[4]; Tullman-Ercek, ed., Danielle; Salmeron-Sanchez, Manuel

Molecular Foundry, Lawrence Berkeley National Laboratory, Berkeley, California, USA
Department of Biosciences, Rice University, Houston, Texas, USA
Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA, Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, California, USA
Molecular Foundry, Lawrence Berkeley National Laboratory, Berkeley, California, USA, Department of Biosciences, Rice University, Houston, Texas, USA

The bacterial extracellular matrix forms autonomously, giving rise to complex material properties and multicellular behaviors. Synthetic matrix analogues can replicate these functions but require exogenously added material or have limited programmability. Here, we design a two-strain bacterial system that self-synthesizes and structures a synthetic extracellular matrix of proteins. We engineered Caulobacter crescentus to secrete an extracellular matrix protein composed of an elastin-like polypeptide (ELP) hydrogel fused to supercharged SpyCatcher [SC^(–)]. This biopolymer was secreted at levels of 60 mg/liter, an unprecedented level of biomaterial secretion by a native type I secretion apparatus. The ELP domain was swapped with either a cross-linkable variant of ELP or a resilin-like polypeptide, demonstrating this system is flexible. The SC^(–)-ELP matrix protein bound specifically and covalently to the cell surface of a C. crescentus strain that displays a high-density array of SpyTag (ST) peptides via its engineered surface layer. Our work develops protein design guidelines for type I secretion in C. crescentus and demonstrates the autonomous secretion and assembly of programmable extracellular protein matrices, offering a path forward toward the formation of cohesive engineered living materials.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1772263

Alternate ID(s):: OSTI ID: 1834354

Journal Information:: mSystems, Journal Name: mSystems Vol. 6 Journal Issue: 2; ISSN 2379-5077

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
Caulobacter crescentus
engineered living material
extracellular matrix
protein hydrogel
protein secretion
surface structures
surface layer protein
type I secretion

Title: Engineering High-Yield Biopolymer Secretion Creates an Extracellular Protein Matrix for Living Materials

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