Exploring Linkages Between Soil Health and Human Health (2024)
Chapter: Summary
Summary
The United States is an important food producer globally, in part because of its abundance of agriculturally productive soils. However, management practices that maximize yields have caused losses in soil organic matter, poor soil structure and water-holding capacity, and increased salinity on millions of acres of land. Microbial communities, the drivers of many soil processes, have been adversely affected by excessive use of tillage, nutrient applications, and pesticides. Erosion, accelerated by tillage and lack of ground cover, has caused the loss of more than 57 billion metric tons of topsoil from the Midwest alone over the past 150 years. Although U.S. agriculture increased its productivity in the 20th century by adopting new practices and technological advances, these increases are not expected to be repeated in the 21st century. Furthermore, the externalized costs to the environment and human health—water and air pollution, biodiversity loss, and increased greenhouse gas (GHG) emissions—caused by many agricultural management practices are apparent and severe.
Considerable efforts are underway to mitigate these problems through management practices that improve soil health, defined by the Food and Agriculture Organization as “the ability of the soil to sustain the productivity, diversity, and environmental services of terrestrial ecosystems.” There is also interest in determining whether improved soil health has favorable effects on the nutrient density of foods grown. Recent advancements have sparked exploration into the interconnectedness of microbiomes across soil, plants, humans, and other animals and how microbiomes can support healthy soils as well as humans. These advances may also lead to new discoveries in the soil microbiome that could facilitate drug development and address threats to human health, including antibiotic resistance, contaminants, and soil-borne pathogens.
Given this, the U.S. Department of Agriculture’s National Institute of Food and Agriculture asked the National Academies of Sciences, Engineering, and Medicine to
convene a committee of experts to explore the linkages between soil health and human health (Box S-1).
THE COMMITTEE’S PROCESS AND SCOPE OF THE STUDY
Members of the Committee on Exploring Linkages Between Soil Health and Human Health were appointed by the National Academies for their expertise relevant to the statement of task. The committee members volunteered for more than a year to write this report, hearing from 33 invited speakers, participating in numerous deliberation sessions, and reviewing and integrating scientific evidence to respond to the statement of task.
The committee approached its task from the viewpoint of the One Health concept—that is, the health of humans, other animals, plants, and the wider environment are linked
BOX S-1
Statement of Task
A committee appointed by the National Academies of Sciences, Engineering, and Medicine will review the state of knowledge on linkages between soil health, with particular respect to U.S. agricultural soils, and human health and prepare a report describing the potential to increase the human health benefits from microbial resources in the soil.
In the course of its review, the committee will identify current research efforts and examine scientific findings on such topics as:
- Relationships between the human microbiome and soil microbiome including the plant microbiome as part of a continuum;
- Linkages between soil management practices and the nutrient density of foods for human consumption and other effects on food;
- Information on soil microbial compounds used in drug development, such as antioxidants, antibiotics, and compounds with anti-cancer properties;
- Information on soil-borne human pathogens and microbial compounds such as toxins;
- Information on the interactions of the soil microbiome with soil contaminants that pose risks to human health; and
- Soil management practices that enhance health benefits and reduce adverse health impacts.
The committee’s report will describe key findings and knowledge gaps, identify promising research directions, and offer recommendations for enhancing the human health benefits of the soil microbiome.
and interdependent. It noted that the pursuit of One Health has, until recently, neglected the environmental piece of the puzzle and that, of the many poorly understood and unintegrated components of the environment, perhaps the most neglected among them is soil. The committee sought to press the One Health treatment of soil beyond its passing inclusion as a medium for food production or a receptacle of chemical contamination and examine the many ways in which the health of soil connects to the health of humans.
Nevertheless, there are many kinds of soils and environments, and the committee could not address all possible linkages between soil health and human health. The committee’s report reflects its statement of task, which was primarily focused on soil used in crop production in the United States. This summary begins with a discussion of linkages between soil microorganisms and human health, followed by the various ways soils and agricultural management practices connect to human health. It also discusses the interplay between management practices, crop nutritional qualities, and possible connections to human health, and it concludes with opportunities for improving human health by increasing soil health. The recommendations made in the report follow each section in Tables S-1 through S-4.
LINKAGES BETWEEN SOIL MICROORGANISMS AND HUMAN HEALTH
Through their ability to cycle nutrients and carbon, filter water, and build soil structure and organic matter, the most obvious linkage between soil microorganisms and human health rests on the fact that they—and soil biota in general—are integral to the capacity of soils to produce food. Perhaps less recognized is the critical role the soil microbiome plays in climate regulation, including carbon sequestration, and the ability of soil microbes to metabolize many organic contaminants into harmless byproducts, which limits exposure to humans. Likewise, many of today’s antibiotics and other drugs are derived from soil microorganisms. That soil microbes can also be harmful to human health is highlighted by several foodborne pathogen outbreaks in fresh produce in recent decades linked to manure or compost-amended soils.
While the above linkages between soil microorganisms and human health are largely known, the connections between soil microbiomes and human microbiomes remain underexplored. There is indirect evidence of the importance of exposure to environmental microorganisms for human health, notably on the immune, metabolic, and central nervous systems. However, the extent to which exposure specifically to the soil microbiome influences the human microbiome is unknown. From animal models, soil biodiversity appears to be interrelated with the mammalian gut microbiome, with studies finding that animals in contact with soil and dust have gut microbiomes with greater diversity and richness. Whether this also occurs in humans and has potential benefits for human health remains unknown.
Additionally, because microbial actions are responsible for many chemical indices currently used as health indicators, the microbiome may provide early indicators of health changes and act as a canary in the coal mine. However, the ability to define and interpret microbial health indicators is currently limited by a sparse understanding of
the ecology and function of microorganisms in both soil and human systems. Sampling and analyzing microbiomes along a continuum of health states and complementary use of multiple molecular (metabolite, proteomic, genomic, and transcriptomic) and non-molecular methods can provide more definitive evidence on microbial metabolic pathways related to health status. This evidence will help researchers incorporate microbiome-related data in future approaches to monitor soil health and human health.
Finally, the reservoir of antibiotics and other medicinal natural products in soils remains largely untapped. Less than 5 percent of the estimated hundreds of thousands of antibiotic substances in soil have been characterized. Continued development of molecular methods and cultivation techniques could offer efficient ways to screen soils for promising medicinal compounds.
LINKAGES BETWEEN AGRICULTURAL MANAGEMENT PRACTICES AND HUMAN HEALTH
Common agricultural management practices have increased crop yield and food security, but this productivity has often come at the expense of soil health, with detrimental effects on the environment and human health. For example, synthetic fertilizer use has greatly increased crop production but has also caused excess nutrients to leach from agricultural fields, sometimes resulting in contaminated groundwater, algal blooms, and production of potent GHGs that contribute to climate change. Although conservation tillage is widely used in the United States, conventional tillage is still employed in many cropping systems and can reduce soil organic matter, suppress biodiversity, and increase erosion. Eroded material can reduce water quality, irritate human respiratory systems, and increase exposure to pesticides and possible contaminants residing in soils. At its most fundamental level, agricultural management practices often create trade-offs between the many services soils provide to people—for example, food production on the one hand and, on the other, the ability of ecosystems to sustain biodiversity, sequester carbon, and perform myriad other functions that are equally, even if less obviously, essential to human health.
Prior to the early 2000s, soils were rarely included in assessments of the services that ecosystems provide to people beyond adequate food and materials for building. Since then, there has been an increasing recognition that soils provide additional important functions. Collectively, these services have been termed Nature’s Contribution to People (NCPs) and include nutrient cycling; water, climate, and air regulation; disease suppression; and habitat creation and maintenance as well as benefits that contribute to cultural, recreational, and spiritual well-being. For example, the world’s soils contain three and four times more carbon than is in the atmosphere and vegetation, respectively, and they play a major role in global carbon cycling through acting as both source and sink.
Management decisions affect whether carbon is stored in or lost from soil. Reduced tillage, increased input of organic matter into soil via crop residues, planting of cover crops or long-lived crops with large root systems, and the use of organic soil amendments (e.g., manure, compost, and biosolids) build soil organic matter and thus carbon in
| Microbiome sampling | Researchers must incorporate sufficient rigor in the sampling design to capture the spatial and temporal heterogeneity of the microbiome to reveal responsive indicators of health. (Recommendation 7-1) |
| Researchers should enhance universal methodologies (sampling, documentation) for microbiome analysis across different sample materials. (Recommendation 7-2) | |
| Microbiome data management | Federal funders should require resources to ensure metadata as well as data on environmental and ecosystem properties or population characteristics be included, properly stored, and reusable, as accessible data are necessary but not enough. (Recommendation 7-3) |
| Microbiome diagnostics | Funding agencies should support discovery of scalable diagnostics, with the goal that affordable, rapid assays will be developed for use on soil microbiomes in the field and with diverse human populations. (Recommendation 7-4) |
| Funding agencies should support research designed to investigate causal relationships in soil and human microbiomes, toward the development of microbial therapeutics. (Recommendation 7-5) | |
| Collaboration | Funding agencies should support microbiome research within disciplines (e.g., community ecology, soil ecology, and soil biogeochemistry or microbiology and medicine) to integrate methodologies to bring together composition and functional assessments of microbiomes. (Recommendation 7-6) |
| Funding agencies should support microbiome research among disciplines (e.g., agronomy, plant science, soil ecology, microbiology, immunology, human nutrition, medicine, engineering) to explore the connectivity of the microbiome across systems (e.g., soil, plants, and humans). (Recommendation 7-7) |
soils. Incidentally, these practices likely also reduce erosion and promote microbial biomass and diversity, nutrient- and water-holding capacity, and aggregate stability. Such changes increase NCPs with direct and indirect benefits to human health, such as water filtration and improved air quality.
Management practices have the potential to assist soils in suppressing plant disease, another soil-derived NCP. Development of disease-suppressive soil is an example of positive plant–soil feedback that can benefit future plant productivity through the lasting effects of plant–soil interactions. Practices that promote microbial abundance and diversity, such as crop rotations, cover crops, residue retention, minimum tillage, and compost or manure addition, have been shown to promote disease suppression.
Along with soil moisture and precipitation, agricultural management practices affect foodborne pathogens and mycotoxin production, both of which present risks to human health. Foodborne pathogens can be introduced to the food supply through organic soil amendments, but there are practices and regulations that mitigate risks to human health. Regarding mycotoxins, the health of soils influences nutrient- and
water-holding capacity of the soil and thus plant stress, which in turn determines the ability of crops to resist colonization. Better understanding of the conditions under which pathogens and mycotoxins thrive will reduce crop losses and human illness by identifying ways to maximize crop growth potential while minimizing practices conducive to pathogen growth or toxin production.
LINKAGES BETWEEN AGRICULTURAL MANAGEMENT PRACTICES AND THE NUTRITIVE VALUE OF FOOD
Although there is a common perception that healthy, well-managed soils produce healthier foods, the connection is not always clear. Nutrient availability in the soil, environmental conditions, management practices, and plant genetics all play a part in determining the nutritional quality of food. Comparative studies of different production systems (e.g., conventional vs. organic) have tried to assess the interplay of these factors, but variations in experimental design, soil types, crop species, and environmental conditions have yielded divergent results. Unfortunately, as with most complex systems where biotic and abiotic factors are at play, the influence of a given management practice on crop yield or nutritional quality is not always predictable or consistent.
What ultimately determines the nutritional quality of food crops is the amount of essential nutrients with health-promoting potential that are transported to, or synthesized within, the edible portion of the plant. These include minerals and biosynthesized macromolecules such as amino acids/proteins, carbohydrates, lipids, vitamins, and phytochemicals (also referred to as bioactive secondary metabolites). Agricultural management practices that modify mineral or water availability can affect crop nutritional quality. Some studies have also demonstrated that enhanced soil organic carbon and microbial biomass are associated with increased levels of phytochemicals commonly associated with reduced risk of chronic diseases in humans. However, such differences largely disappear when edible plant tissue yield is considered. If yields increase, concentrations of certain nutrients and health-beneficial phytochemicals may actually decrease because nutrients do not necessarily all accumulate within edible plant tissues at the same rate. A higher accumulation of yield-increasing macromolecules such as starch or protein may dilute micronutrient concentrations. Nevertheless, an increased crop yield can potentially lead to increased micronutrient content for consumption even if the concentration per unit mass is reduced. Thus, both quality and quantity of harvestable product need to be considered when assessing effects of various management practices.
The lack of a clear relationship between nutritional quality and management practices in studies could also be because the diversity of secondary phytochemicals in plants is complex, and many compounds function as signaling or defensive molecules that can be differentially biosynthesized in response to biotic or abiotic environmental stress. Therefore, a reduction in plant stress may in some instances lead to lower concentrations of these phytochemical compounds in plant foods. Variation in nutritional quality is also highly dependent on plant genetics, and studies of crop genetic diversity have shown broad ranges in nutrient density. Furthermore, plant genetic traits that confer enhanced
| Managing trade-offs and enhancing soil-derived Nature’s Contributions to People (NCP) | The U.S. Department of Agriculture (USDA) and other agencies should prioritize research to better characterize and monitor NCPs (e.g., nitrogen cycling or the nonmaterial NCPs related to human health), to understand the underlying mechanisms to improve predictions (e.g., disease suppression), and to assess their importance across different scales (e.g., plot to landscape and upward). This research should be translated into tools that can be used by land managers in agricultural and nonagricultural settings to inform decisions that involve trade-offs among NCPs. (Recommendation 3-2) |
| USDA, the U.S. Geological Survey, and other agencies involved in land management should support research that explores the mechanisms driving soil-derived regulating NCPs and approaches through which their benefits can be enhanced. (Recommendation 3-4) | |
USDA and other agencies should support research that:
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| Food safety | USDA’s National Institute of Food and Agriculture and the National Institutes of Health should support research studies conducted in controlled environments as well as in field trials that assess persistence of microbial pathogens under varying climatic conditions in order to better understand factors that may facilitate pathogen survival in soil and transfer onto crops. These studies should incorporate various crops, as well as biostimulants and fertilizer additions, that may alter plant–pathogen interactions and zoonotic pathogen persistence. (Recommendation 5-7) |
| USDA should support efforts, such as the USDA–Agricultural Research Service’s National Predictive Modeling Tool Initiative, that use soil monitoring data linked with climate and other environmental data to predict and help control mycotoxin risk in crops and forage species. (Recommendation 5-8) |
micronutrient uptake from soils do not always translate into enhanced accumulation in edible parts. Identifying practical strategies to enhance (micro)nutrient density in staple food crops remains a challenge, especially for at-risk populations in developing regions of the world. This is less of an issue in the United States due to low-cost micronutrient supplementation in staple products (e.g., cereals, dairy, and beverages) and overall diversity in the diet, although micronutrient limitations in soils can reduce yield.
Discussion of nutrient density and phytochemical composition in edible plant material is incomplete without acknowledging the processes that harvested crops undergo before consumption. Nearly all commercially harvested plant foods are processed to make them safe to consume and improve their palatability and shelf life, which alters the nutritional and health attributes. For example, milling cereal grains often removes bran and germ tissues that contain many of the health-beneficial phytochemicals, dietary fiber, minerals, and vitamins. Although nutritional and health benefits of these components are known, capturing their benefits to broadly affect human health remains challenging due to low consumer acceptance of such products. Deriving the full benefits of nutritionally beneficial plant commodities requires innovations in methods to
| Agricultural management practices and food composition | The U.S. Department of Agriculture’s National Institute of Food and Agriculture (USDA–NIFA) and the National Science Foundation (NSF) should support translational research to better understand the effect of different agricultural management practices, when used in specific environments, on the nutrient and bioactive density of crops (in the context of yield) consumed by humans. (Recommendation 5-1) |
| USDA–NIFA, NSF, and the National Institutes of Health should cooperate to support research on the biosynthetic pathways and the environmental cues (including soil factors) that influence food composition, so that crops can be managed or bred for higher levels of target compounds (especially bioactives) even in the absence of promotive environmental signals. (Recommendation 5-2) | |
| USDA–NIFA and NSF should support research, from greenhouse to field scales, to better understand the utility of biostimulants for nutrient uptake and yield under field conditions and considering different ecological factors, including the indigenous soil microbiome. (Recommendation 5-3) | |
| Role of food processing and food choice | USDA–NIFA and private industry should support research in food-processing technologies that enhance the profile of health-beneficial nutrients and bioactive compounds in foods without sacrificing consumer acceptability and that lead to improvements in diet-related indices of public health. (Recommendation 5-4) |
| USDA–NIFA and NSF should support efforts to study the survival and microbial fitness of commensal organisms in foods, their response to thermal and nonthermal processes, and their potential impact on host microbiomes. (Recommendation 5-6) | |
| USDA–NIFA is encouraged to support studies that examine consumer willingness to purchase foods that are more nutrient dense and consumer interest in paying for foods produced with agricultural management practices that support soil health. (Recommendation 5-9) |
minimize losses of such nutrients and bioactive compounds during processing while maintaining consumer acceptance.
Other food-processing technologies, such as thermal treatment or fermentation, can enhance bioaccessibility or bioavailability of some nutrients and phytochemicals. Bacteria in fermented food may even favorably influence the composition of the gut human microbiota in some cases. However, these treatments may also lead to the degradation and loss of nutrients or phytochemicals. Thus, it is always important to consider the final form of edible plant tissue that is consumed when evaluating soil–plant–human health interactions.
IMPROVING SOIL HEALTH TO IMPROVE HUMAN HEALTH
A healthy soil sustains biological processes, decomposes organic matter, and recycles nutrients, water, and energy, reducing the need for synthetic fertilizers and irrigation. It helps mitigate exposure to some chemical contaminants and sustains food production. All these functions make the prioritization of soil health for human health benefits even more important in the face of climate change, which will adversely affect soil nutrient cycling and exacerbate the detrimental effects of flooding or drought on soil stability and water-holding capacity.
Yet, assessing a soil as “healthy” is complex and hotly debated. Numerous variables can be measured, and it is not always clear which ones best correspond to the concept of soil health and how they should be compiled and compared. Consensus has been reached that soil health assessments are regional and system specific and require multiple variables, but which soil health indicators are useful to measure in each context remains contested even as tools have advanced. Furthermore, the spatiotemporal heterogeneity of soil means that single point measurements are unlikely to provide meaningful data for informing management actions or for comparisons across soils. Opportunities exist for monitoring, collecting, and analyzing data so that soil health indicators can be validated over time and in their agricultural context to advance their utility. Such approaches could also be applied to gain a better understanding of the underlying mechanisms contributing to soil health and associated benefits to human health.
Nonetheless, some generalities are possible. A healthy soil will possess optimal pH, nutrient levels, and soil organic matter, with low concentrations of harmful chemicals. Physical properties should provide good aeration and water infiltration and storage. It is increasingly apparent that biodiversity maintenance is an essential constituent for soil health, prompting the urgent need to preserve soil microorganisms (as well as meso- and macrofauna). It is also widely acknowledged that agricultural management practices that minimize disturbance and maximize crop biodiversity, maintain continuous living plants, and keep the soil covered, wherever possible, will build soil health. The incorporation into planting rotations of cover crops, perennial crops, or crops bred specifically for root system development or rhizosphere interactions with soil biota are all options for increasing belowground biomass. More research and development will be needed to make these crops viable choices in the diverse soils and climates of the United States.
TABLE S-4 Recommendations to Improve Soil Health
| Awareness and preservation | Federal agencies and scientific societies should continue their work to promote the public awareness of the importance of soil health and its societal value beyond its immediate material benefits. (Recommendation 3-1) |
| Land managers and city planners should manage landscapes in a way that preserves and promotes soil habitat and biodiversity by minimizing disturbance and soil sealing and optimizing plant cover and diversity wherever possible. (Recommendation 3-3) | |
| Producers and other land managers should adopt practices that increase the organic matter content, biodiversity, and other health parameters of their soils. (Recommendation 6-7) | |
| Agricultural soil management |
The U.S. Department of Agriculture (USDA) should develop a coordinated national approach to monitor soil health over time and space. This approach would allow for broad comparisons across locations and an ability to identify areas of concern. Over time, it would also enable comparisons among management practices as well as their context dependency. To achieve this would require:
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| (Recommendation 4-1) | |
USDA should fund research projects that:
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USDA’s Agricultural Research Service should pursue and USDA’s National Institute of Food and Agriculture (NIFA) should support plant breeding research that improves:
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USDA farm-support programs should consider the benefits of soil health as a context-specific metric of success in restoring degraded soils and as a tool to monitor vital soil functions rather than solely focusing on yield outcomes from management practices and should provide assistance for land managers to support transition to more complex systems. Such assistance could include:
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| (Recommendation 4-5) | |
| Contamination concerns | Federal agencies should work collaboratively to support surveys of soil chemical contaminants informed by systematic risk assessments to identify where contaminant levels in soil may be particularly high (e.g., locations around, downwind, or downstream of PFAS point sources). These surveys can be used to build contaminant maps (e.g., of lead, arsenic, persistent organic pollutants) that can be viewed individually or overlaid to assess the status of contamination, identify locations of concern, and, over time, evaluate the effectiveness of interventions. (Recommendation 6-1) |
| Federal agencies should support interdisciplinary research to reduce gaps in knowledge about exposure pathways from soil and the compounding health effects on soil biota, plants, and people from exposure to multiple chemical contaminants. (Recommendation 6-2) | |
| The United States should mitigate the entry of plastic and PFAS contaminants into soil by reducing their overall production and use. (Recommendation 6-3) | |
| The U.S. Environmental Protection Agency (EPA) should continue pursuing research and technology to remove PFAS from wastewater and biosolids. (Recommendation 6-4) | |
| EPA should pursue research to establish a threshold for plastics in land-applied soil amendments. Revisiting heavy metal thresholds would also be in order. (Recommendation 6-5) | |
| Recycled resources | USDA–NIFA and the National Science Foundation should support research on technologies that enhance usability of food-processing byproducts as functional food ingredients, sources of valuable bioactive compounds and nutrients, or substrates for production of novel high-value compounds. (Recommendation 5-5) |
| Public sector investment should be made to develop affordable technologies for converting biosolids into biochar that can be applied to agricultural land and/or used for wastewater treatment. (Recommendation 6-6) | |
| Public and private entities should invest in Green and Sustainable Remediation techniques, including the application of designer biochars and biosolids biochar, to manage soil contamination effectively. (Recommendation 6-8) |
Although there are many intricacies about soil health to be learned, immediate action should be taken to map and mitigate current soil chemical contamination. The degradation of chemical contaminants is a soil-derived NCP, but contamination can overwhelm the capacity of soil to mitigate risks to human health. High levels of lead and cadmium in soils reduce microbial activity and plant biomass. Microplastics can change soil structure, affect water-holding capacity, and may enrich pathogens and antibiotic resistance genes in soil microbial communities. Per- and polyfluoroalkyl substances, a large group of synthetic, organofluorine chemicals that are highly persistent in the environment, are of increasing concern as environmental contaminants. These and other soil contaminants have not been strategically mapped in the United States. Thus, there is a lack of comprehensive knowledge regarding the geographic distribution of these contaminants in U.S. soils and the specifics of their co-occurrence in mixed forms. Each contaminant class is diverse with heterogeneous impacts based on the nature and quantity of the material and the characteristics of the soil in question. The reality of soil contamination is even more complex because of the potential for co-contamination with multiple compounds. It is likely that contaminants interact with one another in ways that compound the adverse effects on soil health. This gap in understanding underscores the need for more detailed research and mapping of soil contaminants to better address soil and environmental health challenges.
Finally, there are abundant underutilized organic resources in the United States—food waste, compost, agroindustrial and forestry byproducts, manure, biosolids, and source-separated human excreta—that could be used to increase soil nutrients and organic matter and reduce demand for synthetic fertilizer. However, current challenges involving geographic distribution, quantification of nutrient content, and contaminant removal must be solved to make the most effective use of these resources.
GOING FORWARD
The concept of One Health posits that soil should be valued as an ecosystem that, when healthy, contributes to the health of other ecosystems, plants, humans, and other animals and contains a microbiome that connects not only to plants but also likely to people as well. To promote sustainability and resilience, the way soil is viewed must be altered from that of a widget in a production system to that of a component of a holistic system that includes but extends far beyond agriculture. Soil biodiversity must be preserved, both to ensure current soil functions and to safeguard genetic diversity to enable discoveries of future medicines.
This shift in our perception of soil will be guided by a better knowledge of underlying mechanisms contributing to soil health and its connectedness to plant and human health and a continued optimization of ways to quantify and compare health. It will require changes in farm-support programs to value soil health as a metric of success and to transition toward more complex and perennial cropping systems as well as increased circularity where waste streams are turned into safe resources. Finally, societal awareness of the role soil health plays in human health beyond food production must increase, which will require the involvement of many federal agencies, scientific societies, companies, and international organizations.
