Microbiome Engineering: Synthetic Biology of Plant-Associated Microbiomes in Sustainable Agriculture

Abstract

To support an ever-increasing population, modern agriculture faces numerous challenges that pose major threats to global food and energy security. Plantassociated microbes, with their many plant growth-promoting (PGP) traits, have enormous potential in helping to solve these challenges. However, the results of their use in agriculture have been variable, probably because of poor colonization. Phytomicrobiome engineering is an emerging field of synthetic biology that may offer ways to alleviate this limitation. This review highlights recent advances in both bottom-up and top-down approaches to engineering non-model bacteria and microbiomes to promote beneficial plant-microbe interactions, as well as advances in strategies to evaluate these interactions. Biosafety, biosecurity, and biocontainment strategies to address the environmental concerns associated with field use of synthetic microbes are also discussed. Phytomicrobiome Engineering for Sustainable AgricultureThe United Nations estimates world population will be 9.8 billion people by 2050 (https:// population.un.org/wpp/). Agricultural productivity must increase by an estimated 70% to meet increasing demand for food, feed, fiber, and bioenergy (Global Agricultural Productivity Initiative: https://globalagriculturalproductivity.org/). Because arable acreage is unlikely to grow [1], meeting this demand requires achieving higher yields, currently attempted using artificial fertilizers and pesticides whose manufacture and use are not sustainable. Synthetic nitrogen (N) fertilizer production is energy-intensive [2]. Phosphorous (P) and potassium (K) fertilizers are mainly produced from finite mined resources likely to be depleted within 100 years. Pesticides with carcinogenic, developmental, and environmental risks are restricted [3,4]. More sustainable strategies to achieve ever-higher crop yield are urgently needed.Plant-associated microbes harbor enormous potential to provide economical and sustainable solutions to current agricultural challenges. Although plants provide diverse ecological niches for microbes [5,6], microbes provide plant growth-promoting (PGP) traits (see Glossary) for plants [7]. Many PGP microbes have been isolated, and some are widely accepted as biofertilizers, biostimulants, and biocontrol agents (www.cropscience.bayer.com/innovations/agriculturebiologicals/a/hidden-helpers-below-ground). However, applying PGP microbes to fields for commercial adoption has had limited success [8][9][10][11][12]. This is likely because the new microbes are excluded by the more-resilient existing microbial communities [13], whose composition has been shaped over time through complex multilateral interactions with the environment [14][15][16][17][18][19][20]. Finding new microorganisms that can sustainably support plant development, nutrition, fitness, disease control, and productivity in dynamic and stressful environments therefore depends on developing strategies to manage phytomicrobiomes [5,15,[21][22][23][24]. HighlightsMutualistic microbes associated w...

Use of Mineral Weathering Bacteria to Enhance Nutrient Availability in Crops: A Review

“…In a bottom-up approach, selected bacterial strains from the natural community can be genetically modified to carry a desirable trait (i.e., P or K solubilizing ability) and used to assemble a synthetic microbial community. In the top-down approach, desirable traits can be introduced into a range of microbial hosts in situ by gene horizontal transfer using an engineered conjugative donor strain or by bacteriophages (Ke et al, 2020). In the concern of bacterial weathering and rock fertilizers, rational microbiome design could be used to increase weathering traits in soil microbial communities or to introduce other PGP traits and genes for plant colonization/interaction into efficient soil weathering microorganisms.…”

Glutamic Acid Reshapes The Phytobiome To Protect Plants Against Pathogens

“…Trends in plant microbiome studies have approached microbiome engineering with the goal of improving plant health and productivity [26] via either top-down or bottom-up approaches [25]. The top-down approach refers to manipulation of environmental and physicochemical conditions to select the desired biological process [9,27]. This top-down design involves relatively macro-scale processes resulting in microbiome engineering.…”

“…This top-down design involves relatively macro-scale processes resulting in microbiome engineering. Conversely, bottom-up approaches link molecular and biochemical characteristics and relatively micro-scale processes with precise mechanisms in the interaction [27].…”

“…Consequently, these approaches are exible enough to be applied to microbiome-associated phenotypes [27]. In humans or animals, they can be facilitated by prebiotics, a terminology invented in 1995 by Gibson and Roberfroid [28].…”

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