Reconciling Ecological and Engineering Design Principles for Building Microbiomes

Abstract

Simplified microbial communities, or "benchtop microbiomes," enable us to manage the profound complexity of microbial ecosystems. Widespread activities aiming to design and control communities result in novel resources for testing ecological theories and also for realizing new biotechnologies. There is much to be gained by reconciling engineering design principles with ecological processes that shape microbiomes in nature. In this short Perspective, I will address how natural processes such as environmental filtering, the establishment of priority effects, and community "blending" (coalescence) can be harnessed for engineering microbiomes from complex starting materials. I will also discuss how future microbiome architects may draw inspiration from modern practices in synthetic biology. This topic is based on an important overarching research goal, which is to understand how natural forces shape microbial communities and interspecies interactions such that new engineering design principles can be extracted to promote human health or energy and environmental sustainability.

Keywords: community coalescence; ecological processes; environmental filtering; functional trait space; microbial community; microbial ecosystem; microbiome engineering; model system; priority effect; synthetic biology.

FIG 1

Microbiome engineering is an emerging field that draws from both synthetic biology and microbial ecology. Single species and controllable elements of the environment (such as those that can be maintained in cultivation chambers) can be used to build microbiomes via bottom-up approaches (A). In the bottom-up cases, it is easy to conceptualize the modular parts that can be used or reused, manipulated, and shared. However, whole communities and elements of their environment can also be harnessed as modular parts and used or reused as starting materials to select and/or dilute complex microbiomes down to more tractable communities. This top-down approach (B) can be tailored around specific ecological processes harnessed as engineering design principles. One potential frontier in microbiome engineering expands upon the idea of using whole communities (and environmental factors) as modular parts through controlled blending processes that can be defined as directed community coalescence (C). These approaches can be designed to capitalize on common processes that influence natural microbiomes to control/design relationships between functional trait space and taxonomic structure.