Solutions in microbiome engineering: prioritizing barriers to organism establishment

Microbiome engineering is increasingly being employed as a solution to challenges in health, agriculture, and climate. Often manipulation involves inoculation of new microbes designed to improve function into a preexisting microbial community. Despite, increased efforts in microbiome engineering inoculants frequently fail to establish and/or confer long-lasting modifications on ecosystem function. We posit that one underlying cause of these shortfalls is the failure to consider barriers to organism establishment. This is a key challenge and focus of macroecology research, specifically invasion biology and restoration ecology. We adopt a framework from invasion biology that summarizes establishment barriers in three categories: (1) propagule pressure, (2) environmental filtering, and (3) biotic interactions factors. We suggest that biotic interactions is the most neglected factor in microbiome engineering research, and we recommend a number of actions to accelerate engineering solutions.Subject terms: Community ecology, Microbial ecology

Microbiome engineering is a rapidly evolving frontier for solutions to improve human health, agricultural productivity, and climate management. Microbiome engineering seeks to improve the function of an ecosystem by manipulating the composition of microbes. Two major challenges for successful microbiome engineering are (1) the design of a microbiome with improved function and (2) the establishment of an improved microbiome in a recipient system of interest. While multiple articles and reviews have addressed functional design [1–3], microbiome establishment has received less attention. Here, we propose a strategy to improve microbiome engineering by focusing on microbial establishment and leveraging insights from macrobial ecology.Two general engineering strategies are to manipulate indigenous microbes [4] or to introduce new members [5]. The latter involves the design and delivery of inoculants (a.k.a., probiotics in medical and agricultural arenas) and is a rapidly growing biotechnology sector. In their most general form, both strategies have been practiced crudely for thousands of years in human health [6] and agriculture [7]. However, despite current technical advances, inoculants frequently still fail to establish or confer long-lasting (months to years) modifications to ecosystem function [8]. We argue that this repeated failure is in part driven by lack of emphasis on establishment of inoculants.The problem of organism establishment in recipient ecosystems is not unique to microbiome engineering; it has roots in macrobiology, particularly invasion biology and restoration ecology. We propose that adopting a cross-disciplinary conceptual framework to identify barriers to organism establishment, and then prioritizing these barriers through targeted research will accelerate successful microbiome engineering. In addition, recognizing differences in terminology and experimental design within and across disciplines will facilitate research integration across diverse ecosystems and scales. The components of a more holistic strategy are discussed below.