Programmable Bacterial Biofilms as Engineered Living Materials

Abstract

Biological substances like wood and bone demonstrate extraordinary characteristics of “living” features, such as the ability to self-grow, self-heal upon encountering damage, and sense and adapt to environmental changes. These attributes are crucial for their survival and adaptation in complex environments. In the field of material science, there is a growing interest in developing biomimetic materials that can self-monitor, adapt to environmental conditions, and self-repair when necessary. Such capabilities would extend the lifespan of materials and pave the way for intelligent applications. However, creating materials with autonomy and intelligence on par with biological systems remains a daunting challenge. In this context, synthetic biology offers a promising avenue. It not only allows for harnessing the inherent dynamic properties of living organisms but provides the possibility of imparting additional advanced functionalities beyond the reach of synthetic materials systems. This approach enables the integration of living cells into materials, providing them with naturally endowed or artificially designed traits. These innovative materials, known as Engineered Living Materials (ELMs), represent an emerging category of smart materials capable of autonomous functions, with applications varying from biomedicine to sustainable technology.

Microbial biofilms, owing to their dynamic and self-organizing features, serve as an exemplary starting point for developing ELMs. Biofilms consist of complex communities of microorganisms residing within three-dimensional (3D) extracellular matrices known as extracellular polymeric substances (EPS). These matrices offer an ideal blueprint for designing ELMs, attributing to their remarkable stability, enhanced resilience against severe conditions, and genetic programmability inherent in the EPS components. Various biofilm-based living materials have been developed using biofilm components such as extracellular structural proteins, bacterial cellulose, and fungal mycelium, with applications ranging from pollution remediation, building construction, clean energy generation, and biomedicine. Drawing on traits shared with natural living systems, those ELMs are divided into three main groups: self-organizing living materials, environmentally responsive living materials, and living composite materials. Self-organizing living materials are created by genetically altering biofilm components, giving rise to new functions while maintaining the intrinsic hierarchical self-assembling features of bacterial biofilms. Environmentally responsive living materials harboring artificially designed gene circuits enable them to monitor external conditions and respond to particular cues. High-performance living composite materials integrate genetically modified biofilms with nonliving or artificial substances, harnessing the unique features and benefits of both biofilm components and synthetic materials. This account provides an overview of these three categories of biofilm-based living materials, highlighting their respective design strategies and significant applications. By combining principles from materials science and synthetic biology, ELMs offer the potential to create smart materials with adaptive properties. This Account also addresses the challenges and prospects associated with living biofilm materials, intending to spark new ideas and foster interdisciplinary collaborations in this emerging field.