Plants host a mesmerizing diversity of microbes inside and around their roots, known as the microbiome. The microbiome is composed mostly of fungi, bacteria, oomycetes, and archaea that can be either pathogenic or beneficial for plant health and fitness. To grow healthy, plants need to surveil soil niches around the roots for the detection of pathogenic microbes, and in parallel maximize the services of beneficial microbes in nutrients uptake and growth promotion. Plants employ a palette of mechanisms to modulate their microbiome including structural modifications, the exudation of secondary metabolites and the coordinated action of different defence responses. Here, we review the current understanding on the composition and activity of the root microbiome and how different plant molecules can shape the structure of the root-associated microbial communities. Examples are given on interactions that occur in the rhizosphere between plants and soilborne fungi. We also present some well-established examples of microbiome harnessing to highlight how plants can maximize their fitness by selecting their microbiome. Understanding how plants manipulate their microbiome can aid in the design of next-generation microbial inoculants for targeted disease suppression and enhanced plant growth.

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Modulation of the Root Microbiome by Plant Molecules: The Basis for Targeted Disease Suppression and Plant Growth Promotion

Isolated from a wide range of sources, the genus Paenibacillus comprises bacterial species relevant to humans, animals, plants, and the environment. Many Paenibacillus species can promote crop growth directly via biological nitrogen fixation, phosphate solubilization, production of the phytohormone indole-3-acetic acid (IAA), and release of siderophores that enable iron acquisition. They can also offer protection against insect herbivores and phytopathogens, including bacteria, fungi, nematodes, and viruses. This is accomplished by the production of a variety of antimicrobials and insecticides, and by triggering a hypersensitive defensive response of the plant, known as induced systemic resistance (ISR). Paenibacillus-derived antimicrobials also have applications in medicine, including polymyxins and fusaricidins, which are nonribosomal lipopeptides first isolated from strains of Paenibacillus polymyxa. Other useful molecules include exo-polysaccharides (EPS) and enzymes such as amylases, cellulases, hemicellulases, lipases, pectinases, oxygenases, dehydrogenases, lignin-modifying enzymes, and mutanases, which may have applications for detergents, food and feed, textiles, paper, biofuel, and healthcare. On the negative side, Paenibacillus larvae is the causative agent of American Foulbrood, a lethal disease of honeybees, while a variety of species are opportunistic infectors of humans, and others cause spoilage of pasteurized dairy products. This broad review summarizes the major positive and negative impacts of Paenibacillus: its realised and prospective contributions to agriculture, medicine, process manufacturing, and bioremediation, as well as its impacts due to pathogenicity and food spoilage. This review also includes detailed information in Additional files 1, 2, 3 for major known Paenibacillus species with their locations of isolation, genome sequencing projects, patents, and industrially significant compounds and enzymes. Paenibacillus will, over time, play increasingly important roles in sustainable agriculture and industrial biotechnology.

MOESM3 of Current knowledge and perspectives of Paenibacillus: a review

Plant secondary metabolites (PSMs) play many roles including defense against pathogens, pests, and herbivores; response to environmental stresses, and mediating organismal interactions. Similarly, plant microbiomes participate in many of the above-mentioned processes directly or indirectly by regulating plant metabolism. Studies have shown that plants can influence their microbiome by secreting various metabolites and, in turn, the microbiome may also impact the metabolome of the host plant. However, not much is known about the communications between the interacting partners to impact their phenotypic changes. In this article, we review the patterns and potential underlying mechanisms of interactions between PSMs and plant microbiomes. We describe the recent developments in analytical approaches and methods in this field. The applications of these new methods and approaches have increased our understanding of the relationships between PSMs and plant microbiomes. Though the current studies have primarily focused on model organisms, the methods and results obtained so far should help future studies of agriculturally important plants and facilitate the development of methods to manipulate PSMs-microbiome interactions with predictive outcomes for sustainable crop productions.

Linking Plant Secondary Metabolites and Plant Microbiomes: A Review

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

Land degradation reduces soil functioning and, consequently, the services that soil provides. Soil hydrological functions are critical to combat soil degradation and promote soil restoration. Soil microorganisms affect soil hydrology, but the role of soil microbiota in forming and sustaining soil is not well explored. Case studies indicate the potential of soil microorganisms as game-changers in restoring soil functions. We review the state of the art of microorganism use in land restoration technology, the groups of microorganisms with the greatest potential for soil restoration, knowledge of the effect of microorganisms on soil physical properties, and proposed strategies for the long-term restoration of degraded lands. We also emphasize the need to advance the emerging research field of biophysical landscape interactions to support soil-plant ecosystem restoration practices. Description Microbes repairing degraded soils Soils worldwide have become increasingly degraded by human activities, especially in drylands. Land degradation negatively affects soil hydrological functioning and thereby the ecosystem services that soil provides. Soil microbes may play an important part in the restoration of degraded soils, positively influencing moisture content and other physical features of soil. Coban et al. reviewed recent work on soil hydraulic properties, potential groups of microorganisms for hydrological soil restoration based on their resilience in dry soils, and future strategies for long-term restoration of degraded lands. —AMS A review suggests that soil microorganisms may be the key to the restoration of hydraulic function in soils degraded by human activities. BACKGROUND Soil, the living skin of Earth, provides ecosystem services critical for life: Soil acts as a filter and store of water, provides a growing medium that supplies plants and heterotrophs with water and nutrients, offers habitat for a large diversity of organisms, and is the source of most of our antibiotics. Humanity is increasingly challenged by the combination of climate change, population growth, and land degradation, including carbon loss, biodiversity decline, and erosion. In particular, land degradation reduces soil hydrological functioning and thereby several other ecosystem services. Such impacts occur through alterations of hydraulic functioning, infiltration and soil moisture storage, carbon cycling, biological activity, transport of nutrients and contaminants, and plant growth. Impacts of global environmental change and associated soil degradation need to be understood and reversed as biodiversity, food production, climate regulation, and people’s livelihoods are increasingly affected by soil ecosystem degradation. The interplay between soil biota and soil hydrological functioning plays an essential role in many biogeochemical cycles, including the water and carbon cycles. Microorganisms dominate soil life and perform an array of vital soil functions by regulating nutrient cycling, decomposing organic matter, defining soil structure, suppressing plant diseases, and supporting plant productivity. The presence of microorganisms and their activity can affect soil structure and hydraulic properties in multiple ways. Case studies indicate the potential of microorganisms as game-changers toward the restoration of soil functioning. However, the role of soil microbiota in forming and sustaining soils has historically been overlooked. ADVANCES It has been proposed that microbial communities not only are an indicator of ecosystem health and restoration level but also can be manipulated to enhance the recovery of degraded ecosystems. In the past decade, there have been an increasing number of studies suggesting the use of microorganisms as ecosystem mediators, particularly to enhance crop production and to engineer microorganisms for dryland restoration. Most current experimental approaches focus on monitoring changes in the microbial community that can be correlated with land restoration; however, microorganisms are also facilitators of ecosystem change, not just followers. We review how microorganisms can help address different types of land degradation, with a focus on physical soil loss and transformation, loss of soil chemical properties, and contamination. We discuss potentially the most valuable groups of microorganisms for soil restoration (namely, plant growth–promoting rhizobacteria, nitrogen-fixing bacteria, and mycorrhizal fungi), emphasizing drylands and advances in plant-microbe interaction studies. We review known effects of microorganisms on soil physical and, specifically, hydraulic properties at pore scale and discuss future strategies for the long-term restoration of degraded lands. We also identify the methodological challenges that have so far hampered progress in understanding soil biophysical processes. OUTLOOK Microorganisms can play the leading role in restoring degraded lands, improving soil hydraulic properties such as infiltration and water retention and reducing soil hydrophobicity, which together can facilitate ecosystem restoration. We advocate for research on mechanisms to restore degraded soils with the use of microorganisms. Given the critical role of freshwater availability to terrestrial life and the paucity of studies on hydrological restoration, we especially advocate for research on the hydrological restoration of degraded soil using microorganisms. We propose that microorganisms can improve soil hydraulic properties such as infiltration and water retention and reduce soil hydrophobicity. Along with new organic matter derived from microbes, this will promote plant growth and facilitate further ecosystem restoration. Such a restoration strategy requires collaboration across the research fields of microbiology and soil hydrology, of which there has been very little to date. Understanding the dynamics of soil microbes and connected hydrological processes would create the foundation for restoration practices that can return resilience to the soil ecosystem. Degraded land in Libya. In degraded lands, a decrease in soil nutrients and organic matter, deterioration of soil structure, increase in salinity, water deficiency, and physical instability can be observed. Credit:cinoby/istockphoto

Michael Rothballer

Papers

Systems Biology of Plant-Microbiome Interactions