1
Introduction
The United States is a large producer of food on the global stage. Its volume of production has many contributing factors, but one of the foundations of the U.S. agricultural sector is the abundance of agriculturally productive soil found within its borders. More than a third of U.S. soils are categorized as Mollisols or Alfisols, the two soil orders considered to be most productive in terms of crops (Eswaran et al. 2012).1 Mollisols are rich in organic matter from the growth and decomposition of deep-rooted perennial grasses that grow in them, while the clay content of Alfisols, which formed under deciduous forests, holds water and nutrients in the root zone (USDA–NRCS 1999; Eash et al. 2008; Eswaran et al. 2012; Parikh and James 2012). Mollisols comprise the Palouse region of the Pacific Northwest, whereas much of the soils of California’s Central Valley are Alfisols. Soils of both orders dominate the Great Plains and Midwest. The fertility of these soils, assisted by irrigation, drainage, or both in some areas, is a substantial component in the success of the U.S. agricultural sector (U.S. Bureau of the Census 1952).
Yet, the productivity of U.S. agriculture since the mid-20th century is, to a large extent, decoupled from the historic richness of the soil. Erosion—accelerated by tillage and from leaving the land bare for parts or all of the year—is estimated to have caused the loss of more than 57 billion metric tons of topsoil (and the nutrients and organic matter therein) from the north central states since the 1870s (Pimentel 2006; Thaler et al. 2022).2 Following decades of tillage with moldboard plows, monoculture cropping patterns, and the regular removal of crop residues from harvested land, Donigian et al. (1994) calculated that, by the 1950s, the amount of organic carbon in soils in the middle
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1 The U.S. Department of Agriculture has categorized soil into 12 orders based on measurable and observable soil properties. See USDA–NRCS (1999) for more information.
2 Parts of North Dakota, South Dakota, Nebraska, Kansas, Minnesota, Missouri, Wisconsin, Illinois, Indiana, and all of Iowa.
of the country—from North Dakota and Nebraska in the West to Pennsylvania in the East and south to Oklahoma, Arkansas, and the northeast corner of Alabama—was half what it had been in 1907. Reduced water-holding capacity of soil due to the loss of soil structure and organic carbon from erosion, tillage, and removal of crop residue also adversely affects crop productivity (Pimentel et al. 1995; Evanylo and McGuinn 2000). Furthermore, by the 1980s, soil salinity affected 27 percent of irrigated land, nearly 13 million acres, in the United States (Postel 1989).
Soil microbial communities, the drivers of many soil processes, have also been affected. For example, studies conducted on research plots in Michigan and Illinois have found reduced microbial diversity in agricultural soils. A study on the Michigan plots compared uncultivated land and plots under different agricultural management treatments and found that microbial communities in uncultivated land were different in structure from cultivated land, regardless of treatment (Buckley and Schmidt 2001). The experiment conducted in Illinois, at the oldest continuously maintained agricultural research plots in the United States, concluded that fewer rare bacterial taxa, less diversity and richness in bacteria, and more bacteria adapted for low-nutrient conditions were found in the soil of plots that either received no fertilizer or were treated with inorganic fertilizer in continuous corn plantings versus soil in plots treated with cattle manure (Soman et al. 2017). Likewise, frequent tillage and high inorganic nutrient inputs have suppressed the abundance of beneficial mycorrhizal fungi that colonize plant roots, build soil structure, and aid in plant nutrient acquisition, pathogen protection, and drought tolerance (Johansson et al. 2004; Delavaux et al. 2017).
U.S. agriculture overcame this soil degradation and accelerated its productivity in the 20th century by adopting new practices and taking advantage of technological advances. Further declines in soil organic matter content following the 1950s were mitigated by the integration of soybeans in crop rotations even as planting of clover and other leguminous crops declined or plateaued (U.S. Bureau of the Census 1952; Allmaras et al. 1998; Grey et al. 2012), the mid-century switch to mechanized combine harvesters (which left more crop residue on the field than binders or pickers; Allmaras et al. 1998), and the application of synthetic fertilizer, for which the amount used tripled between 1940 and 1960 and steadily increased until 1981 (Hignett 1956; Collier et al. 2017; Hellerstein et al. 2019). The transition from animal power to machines, already underway well before 1950, increased farm productivity and labor efficiency, and investment in and adoption of crops bred to produce high yields when supplemented with applied fertilizer bolstered productivity (U.S. Bureau of the Census 1952; Allmaras et al. 1998; Pardey and Alston 2021). Pesticide use also began to take off in the 1950s, replacing the labor needed to mitigate crop damage from weeds, insects, and pathogens (Osteen and Szmedra 1989). After hitting a plateau in 1920, the number of irrigated acres in U.S. agriculture increased from 1940 until the late 1970s (Hrozencik and Aillery 2021), and new technology—particularly the development of corrugated plastic tubing in the 1960s—lowered the costs associated with draining land (Fouss and Reeve 1987). Between 1948 and 2021, the volume of U.S. crop production increased 190 percent while the amount of labor and land used in agriculture fell (USDA–ERS 2024).
However, the rate of productivity increases in the 20th century is not expected to be repeated in the 21st century. Efficiencies in labor, advances in genetics, and tech-
nological innovations will continue, but the degree to which they increase productivity will likely be smaller (Pardey and Alston 2021). Furthermore, the externalized costs to the environment caused by current agricultural production systems, such as water and air pollution and biodiversity loss, are apparent (Broussard and Turner 2009; EPA 2011; Tibbett et al. 2020).
Many of these externalities, which have implications not only for the environment but also for human health, connect back to the soil. Nutrients applied to the soil that are not taken up by plants or microorganisms leach into groundwater, contaminating drinking water supplies (Capel et al. 2018). Excess nutrients, pesticides, and sediment as well as antibiotics and other contaminants from livestock manure and biosolids leave the field through surface drainage systems or because of extreme rain events, polluting surface waters that are places of recreation for people or that supply drinking water to communities (Capel et al. 2018). More than half of the emissions in the United States of nitrous oxide—one of the greenhouse gases causing global warming—come from cropland, due in large part to the application of synthetic fertilizer and the mineralization of soil organic matter, which increases the amount of mineral nitrogen in the soil (EPA 2023). Loss of function in soil microbial communities, which can be connected to decreases in soil microbial biodiversity (Wagg et al. 2021), affects the biogeochemical cycling of nutrients and the growth of plants, with concomitant deleterious effects on food production and the climate (Saleem et al. 2019). Loss of soil microbial diversity may also affect human health as evidence increasingly supports the importance of environmental exposure to microorganisms in the development of the immune system (Hanski et al. 2012; von Mutius 2021).
There are considerable efforts underway to decrease these external costs and the subsequent adverse effects on human health through management practices that improve soil health while maintaining or even increasing the supply of food produced by U.S. agriculture (e.g., Wolfe 2019; Hills and Benedict 2021; USDA 2022, 2023). At the same time, there is interest in determining whether changing agricultural management practices to improve soil health has a favorable effect on the nutrient density of foods grown in the United States (Carr et al. 2013; Reeve et al. 2016; Montgomery and Biklé 2021; Bourne et al. 2022; White House 2022). Scientific advances in the past 10–20 years that have increased the ability and reduced the cost of exploring the microbiome—across soil, plants, and humans and other animals—are also spurring interest in how microbial communities are connected among species and how attention to microbiomes can support soil health, food quality, and human health. These advances may also lead to new discoveries in the soil microbiome that could facilitate drug development and address threats to human health such as antibiotic resistance, new and emerging contaminants, and soil-borne pathogens (Hover et al. 2018; Gambarini et al. 2021).
With these possibilities in mind, the U.S. Department of Agriculture’s National Institute of Food and Agriculture (USDA–NIFA) asked the National Academies of Sciences, Engineering, and Medicine (hereafter referred to as the National Academies) to convene a committee of experts to explore the linkages between soil health and human health.
THE COMMITTEE AND ITS CHARGE
The committee was asked to review the state of knowledge on linkages between soil health and human health, giving particular attention to the linkages involving the United States’ agricultural soils. Several components of the statement of task called for exploration of the soil microbiome and possible connections to human health. The committee was also charged with providing information about soil-borne pathogens and toxins as well as microbial compounds that could be used in drug development. The sponsoring agency, USDA–NIFA, asked the committee to identify promising research directions and offer recommendations for enhancing the human health benefits of the soil microbiome. The study’s full statement of task is in Box 1-1.
The National Academy of Sciences appointed a committee with the diverse expertise and experience needed to address this specific statement of task. The committee contained experts in agronomy, plant pathology, food science, microbiomes, human
BOX 1-1
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.
nutrition, microbial ecology, soil science, toxicology, and human health. As with all National Academies committees, members were appointed for their individual expertise, not their affiliation to any institution, and they volunteered their time to serve on this committee. The biography of each committee member can be found in Appendix A.
THE COMMITTEE’S PROCESS
The committee carried out its task between April 2023 and April 2024. It held 11 information-gathering meetings between April and October 2023, hearing from 33 invited speakers. All information-gathering meetings, whether conducted online or in a hybrid format, were open to the public, live streamed, and recorded and posted on the study’s website. Agendas for these meetings can be found in Appendix B.
The committee reviewed relevant scientific literature as well as written comments provided by the public. All materials submitted to the committee by members of the public were archived in the study’s public access file.
Over the course of several months, the committee drafted a report in response to the statement of task. This draft was then reviewed anonymously by experts with knowledge complementary to those serving on the committee. The committee members revised the report on the basis of the reviewers’ comments. This process was overseen by the National Academies’ Report Review Committee. The report was made publicly available after the Report Review Committee determined that the committee had appropriately addressed the reviewers’ comments.
SCOPE AND ORGANIZATION OF THE REPORT
This report is not the first time a National Academies committee has been asked to explore soil health in the context of agriculture. The most direct antecedents include Alternative Agriculture (NRC 1989), Soil and Water Quality: An Agenda for Agriculture (NRC 1993), Toward Sustainable Agricultural Systems in the 21st Century (NRC 2010), and Science Breakthroughs to Advance Food and Agricultural Research by 2030 (NASEM 2019). These reports all touched on the human health implications of agricultural soil management, but the linkages between soil health and human health were not directly in their remit. Other reports have examined the connection between specific soil management practices (in agriculture and beyond agriculture) and human health.3 This report reiterates many conclusions and recommendations made in the past reports.
The committee’s statement of task also builds on previous National Academies’ reports on the microbiome and the technologies that can be used to understand it. In particular, the 2007 report The New Science of Metagenomics presaged the opportunities of new technologies to understand microbial life (NRC 2007). This report is the
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3 See, for example, Use of Reclaimed Water and Sludge in Food Crop Production (NRC 1996), Biosolids Applied to Land (NRC 2002), and Bioavailability of Contaminants in Soils and Sediments (NRC 2003).
first by the National Academies to focus explicitly on the microbial life in soil since the -omics revolution.
Given the emphasis placed on the soil microbiome in the statement of task, the committee devoted substantial discussion in Chapter 2 to the biological properties of soil, the microbial diversity found in soil, and the interactions between soil microbial communities and plant microbial communities. This discussion is placed within a wider context of the importance of soil in the objectives of One Health and the influence that global change events, such as land use change and global warming, have on soil properties (lower right corner of Figure 1-1).
The statement of task asked the committee to examine linkages between soil management practices and the nutrient density of foods as well as how these practices could enhance human health benefits and reduce adverse health impacts. Therefore, Chapter 3 reviews the contributions that soil makes to human health in terms of the ecosystem services it provides. These include material and nonmaterial contributions as well as regulating services, such as water filtration and carbon cycling (left side of Figure 1-1). Interpreting soil management practices to involve those related to crop agriculture, the committee describes the effects of agricultural management practices on soil health in Chapter 4. Tillage, irrigation and drainage, crop choice and land cover, synthetic fertilizer use, organic soil amendment application, and pesticide use are specifically reviewed (top right corner of Figure 1-1). This chapter also reviews indicators used to assess soil health. This discussion of agricultural management practices then sets up the exploration in Chapter 5 of the evidence for the linkages between agricultural management practices and the nutrient density of food. Chapter 5 also examines how food-processing technologies and consumer dietary choices complicate efforts to trace a line from healthy soil to healthy food.
Soil-borne human pathogens are numerous and not limited to agricultural settings. The committee did not deal with them extensively. Soil-borne human pathogens merit their own treatment, but they are not directly relevant to agricultural management practices in farming systems, aside from those that cause food-safety issues. The effects of agricultural management practices and soil health on foodborne pathogens and mycotoxins are addressed in Chapter 5.
Similarly, the committee recognizes that human health is affected by chemical contaminants found in soil through exposure in situations other than agricultural settings or food consumption and that agricultural management practices are not the only source of soil contaminants. Soil contamination has been addressed by the National Academies in previous reports (NRC 1996, 1997, 2003, 2005). In this report, the committee limits its analysis, for the most part, to examples of heavy metal contaminants that may affect human health through food consumption in Chapter 6. Microplastics and per- and polyfluoroalkyl substances (PFAS) are also reviewed as they are emerging contaminants of soils (middle right of Figure 1-1). However, the committee notes that these emerging contaminants are ubiquitous in households and in the environment and that soils are not the only route of exposure.
The field of microbiome science is rapidly advancing. Chapter 7 looks at what the tools available today can reveal about the soil microbiome, the human microbiome, and
connections between the two. It identifies the steps needed to turn the immense amount of data available about microbiomes into actions to improve soil health and human health. Chapter 8 summarizes the committee’s conclusions and recommendations for research directions.
The committee recognizes that agriculture in the United States is comprised of diverse farming systems that exist in a variety of soil types in different scales, climates, and topographies. It is not possible for the committee to address agricultural management practices for all systems or all crops. Therefore, this report is primarily concerned with soil health in larger cropping systems. Urban agriculture is addressed briefly in Chapter 4; however, the issues of soil health and its relationship to human health in urban agricultural systems and in urban soils generally in the United States are unique enough to deserve their own treatment. Similarly, soil health in forage systems is discussed in Chapters 4 and 5, but livestock and pasture systems are not covered extensively. The committee also is aware that soil management practices can have adverse effects on human health for those who work with soil (e.g., farmers, farm workers, and landscapers), but this report does not address occupational health concerns.
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