How microbes can help feed the world.
Extracts of a report from the American Academy of Microbiology.
This report is based on deliberations of experts on how plant microbe interactions could be employed to boost agricultural productivity in an environmentally friendly way.
According to the United Nations World Food Program, more than 870 million of the world’s people are malnourished. Most of the hungry are children. In the developing world, malnutrition contributes to the death of 2.6 million children each year and one of six children is underweight. At the same time that more food is desperately needed, arable land and important resources like fertilizer and water are limited. Salinization and climate change also limit the suitability of much land for agricultural production. Feeding a global population that is projected to reach 9 billion by 2050 will require that agricultural yields increase by 70-100%.
Yields of any given crop vary widely from place to place, even in the same region. Those who study global agricultural trends speak of the ‘yield gap’, which is the difference between the best observed yield and results elsewhere. Theoretically, if we could close the yield gap — if all farmers could achieve the highest attainable yield — worldwide crop production would rise by 45-70%. Yield gaps can often be explained by inadequate fertilizer or water, or by losses to pests or disease. Vast increases in the use of fertilizers, water, and pesticides are not only economically impractical, but would have many negative environmental consequences. Scaling up current high-input agricultural systems is simply not feasible.
But what if the yield gap could be closed in another way, if yield could be increased with dramatically fewer chemical inputs? Producing more food with fewer resources may seem too good to be true, but the world’s farmers have trillions of potential partners that can help achieve that ambitious goal. Those partners are microbes.
Microbes and plants are intimate partners in virtually every life process.
Microbes already help feed the world. In fact, without microbes there would be no plants or animals, as all life on Earth is dependent on microbes to provide many essential services. Increasingly, biologists are recognizing that all multicellular organisms from sponges to termites to humans are dependent on intimate, evolutionarily-ancient relationships with many different kinds of microbes. For plants, vulnerable as they are to changes in their immediate environment, the services provided by microbes are critical. In their natural, unmanaged environments, all plants are supported by a vast, invisible world of bacteria, viruses, and fungi that live in and around their roots, stems, leaves, seeds, pollen, fruits, and flowers.
Additional complex communities of microbes live in and on the insects, birds, invertebrates, and other animals that interact with plants and with each other. These interlocking, interdependent communities have deep evolutionary roots, reaching all the way back to the origin of multicellular organisms and the emergence of land plants and animals. Their diversity and capabilities are nothing short of astounding.
Microbes support plant health by increasing the availability of nutrients, enhancing plant root growth, neutralizing toxic compounds in the soil, making plants more resistant to disease, heat, flooding, and drought, and deterring pathogens and predators. Microbes and plants are intimate partners in virtually every life process. Microbial communities that help the plants overcome these environmental challenges.
Some of the ways microbes contribute to plant health have been known for a long time, and new ones regularly continue to be discovered. Recently, a realization has begun to take hold that these relationships are more vast and important than previously recognized. In the past 20 years or so, our ability to study these complicated communities and unravel the detailed mechanisms by which the members interact has improved enormously.
Optimizing the microbial communities of plants offers an entirely new approach to enhancing productivity.
Increasing our knowledge of plant-microbe interactions has deep implications for agriculture. When humans domesticated plants and animals thousands of years ago, they did so without any knowledge of the local microbial communities that were essential to the health and productivity of those plants and animals. Multiple strains of wheat, corn, rice, and other crops have been planted around the world in environments where the local microbial communities differ from those where the plants originated, and where conditions are such that the plant might need new microbial partners to grow best. Optimizing the microbial communities of plants offers an entirely new approach to enhancing productivity. Indeed, such an approach is the opposite of past management strategies that targeted microbes in the mistaken belief that they all cause disease.
Some beneficial microbes have been known for a long time; the microbes known as Rhizobia that inhabit the roots of leguminous plants and provide them with usable nitrogen, were described by Martinus Beijerinck in 1888. Other observations, for example, that certain plant diseases seemed to be rarer in some fields than others, led to research that showed that the “disease suppression” was due to living organisms. Even before the responsible organisms were identified, farmers could move soil from one field to another to take advantage of its protective abilities.
Virtually every aspect of plant biology is affected by interactions with microbes.
In the last fifty years, a great deal has been learned about a few of the microbes that live in, on, and near plants. In the last ten years, scientists have made tremendous progress in describing the incredible diversity of this microbial world, and have begun to dissect the elaborate networks of communication and cooperation among plants, insects, invertebrates, grazers, and microbes, and determine the precise molecular mechanisms of such interactions. Commercial applications of these discoveries are already being used to support plant growth, health, and productivity. However, the as-yet-unrealized benefits of understanding how microbes support plant vitality could be immense. Simply recognizing that our major crop plants have been bred and cultivated without attention to their ancestral microbial partners is in itself potentially revolutionary in its implications. The possibility exists of an array of agricultural practices and products that could increase the productivity of any crop, in any environment, in an economically viable and ecologically responsible manner.
The ubiquity and diversity of plant-microbe interactions can seem almost overwhelming, especially since science has barely scratched the surface of these fundamental biological partnerships. The potential for societal gain is so high, however, that this crucial field of study will richly reward additional attention and investment.
Why do plants need microbes?
When we think about a corn plant or an apple tree, it seems straightforward to list the factors that affect their health and productivity: sunlight, water, reasonable temperatures, and fertile soil. But in nature, these factors are rarely found altogether at all times. How then do plants survive when one or another of these factors is absent or limited for some period of time? The answer is that there is another, mostly invisible, but crucially important, ingredient involved in the well-being of every plant. Virtually every aspect of plant biology is affected by interactions with microbes. Given fluctuations in the natural environment, plants literally could not survive without microbes and therefore all plants form a multitude of relationships with many different kinds of microbes. Some of these relationships are essential and enduring, others are transient or needed only in certain circumstances.
The relationships between plants and microbes date back to the origin of plants. The early evolution of plants took place in an extraordinarily diverse microbial world; bacteria, archaea and viruses had been evolving for billions of years and occupied every conceivable environmental niche. A new partnership between eukaryotic cells and cyanobacteria led to the acquisition of chloroplasts and set the stage for the evolution of plants. This transformative evolutionary event allowed plants to break into the crowded microbial world by co-opting the ability of cyanobacteria to turn sunlight and carbon dioxide (CO2) into easily digestible sugars, and using that ability to drive the evolution of a myriad of multicellular forms that could carry out that reaction at much larger scales and store the resultant fixed carbon for the next generation. While chloroplasts may be the most ancient evidence of the intertwined evolutionary trajectories of plants and microbes, there are many examples of other long-standing evolutionary relationships, of which the mutualistic symbiosis between leguminous plants and nitrogen-fixing rhizobial bacteria is probably the most familiar, though by no means the most common.
Plant-microbe interactions are not limited to bacteria. Plants have intimate, longstanding relationships with viruses and fungi as well. The ability to carry out photosynthesis and store that energy in the form of leaves, fruits, tubers, and roots makes plants a highly attractive food source. Light and CO2 are not the only inputs plants need; they also require a regular supply of water, as well as nutrients like nitrogen and phosphorus, and trace minerals. How do they acquire those inputs, without being able to travel to find them?
In short, there is a great deal of communication going on and we are just beginning to realize how important it is. A goal for the future is to be able to listen in ourselves.
A multitude of mutually beneficial relationships in which the plant provides shelter or sugars and the microbe provides nutrients or protection from pathogens have evolved over time. The number of recognized microbe-plant interactions is large and growing all the time and they can be classified in several different ways. Most importantly, while we are becoming increasingly aware of mutually beneficial relationships, interactions between plants and microbes can also be neutral or harmful. The conceptual shift that needs to take hold is that plant health is intimately tied up with a complex and largely invisible ecosystem in which literally thousands of species are competing or cooperating in response to constantly changing environmental conditions.
Microbial plant partners
There are three major groups of microbes associated with plants. The kinds of services they provide to plants overlap in many ways and may be provided by a single type of microbe or by more than one of them working together. The relationships among these microbes themselves may also be beneficial, neutral, or antagonistic.
Bacteria are fantastically abundant; there are up to 1010 bacterial cells per gram of soil in and around plant roots, a region known as the rhizosphere. Bacteria are also tremendously genetically diverse — that same gram of soil may contain up to 10,000 different species of bacteria. In addition to the soil, many other bacterial species occupy a variety of niches on and within the aboveground parts of plants.
Among the many services that bacteria can provide are: acquisition of nutrients and minerals; production of antibiotics to deter pathogens and toxins to deter pests; and production of hormones and other compounds to spur growth, stimulate the immune system, and modulate responses to stress. Bacteria also participate in complex communities in which one member may secrete a signal that attracts beneficial organisms, another may ward off pathogens, and still another may produce a substrate upon which other beneficial microbes feed. Together these communities may form dense structures called biofilms that have distinct members and properties, serving, for example, as communication and transportation networks.
It has recently become clear that the number and diversity of fungi associated with plants is more vast than previously appreciated. There are 105 to 107 fungal cells per gram of soil, and that reflects only part of the story because fungi live not only on or around plants, but also within them. Every plant that has been sampled has one or many endophytic fungi. The fungi have been found in association with most plant tissues, living between and within plant cells, and forming extensive networks of which only some functions are known. These fungal symbionts form long filaments, or hyphae, that act as extensions of the plant’s roots and are critical in the acquisition of nutrients, minerals, and water. Endophytic fungi can also be found in above-ground plant tissue. For example, Clavicipitaceae endophytes form intercellular networks within their partner grasses where they produce toxins that ward off insect pests and grazing animals. An emerging consensus asserts that many plants in extreme environments survive only because they have formed partnerships with fungi that provide essential tools to survive heat, drought, salt, heavy metal, and other stresses.
Of the many microbes upon which plants are increasingly recognized as being dependent, perhaps viruses are the most surprising. Viruses are far and away the most numerous biological entities on Earth. Every living organism can be infected by at least one and usually many viruses, and most organisms are infected by a diverse and unexplored collection of viruses. However, viruses are rarely considered outside of their role as pathogens. This is understandable; viruses were discovered because of their role in disease. The idea that viruses might be contributing to the healthy state has been slow to emerge. Gradually, though, examples are accumulating of situations where viruses are not only beneficial, but may be essential to some plants.
The ecological approach that plants themselves have used to overcome environmental challenges has been almost completely ignored.
The ability of viruses to affect plant phenotype is well-known to plant breeders, as it is a virus that produces the streak or flame-like markings in tulip flowers. During the tulip breeding craze in 17th century Holland, breeders knew that they could introduce the streaks by grafting bulbs of striped and plain tulips together. They also knew that the striped varieties gradually declined in health and could not be maintained permanently. But it was only in the 1920’s that the “tulip breaking virus”was identified as the reason behind striping. The first virus identified (in 1898) was tobacco mosaic virus, and there are now about 1000 classified plant viral pathogens. But plant viruses have largely been identified because they are causing damage; the idea that some plants may be thriving because of viruses they carry is a relatively new one.
Studies have shown that many plant viruses that cause disease under benign conditions act to improve tolerance when plants are drought stressed. In some cases viral infection may be essential for survival under stressed conditions; the panic grass that grows in the hot soils of Yellowstone National Park can only survive if it carries a certain fungus that is itself infected by a virus. Many plants and fungi carry persistent viruses that are passaged vertically for indefinite time periods. These may serve as cytoplasmic epigenetic elements, providing novel genetic information beyond the plant and fungal genomes.
The theme that carries through all of these examples of beneficial plant-microbe interactions is that over billions of years plants have formed partnerships with a variety of microbes to allow them to survive when environmental conditions are not ideal. When levels of nutrients or water are inadequate, when temperatures are too high or too low, when competitors, predators, or pathogens threaten, often plants have been able to draw on microbial partners to overcome these challenges.
The implications of this realization for agriculture are profound. For millennia, farming practices have sought to provide ideal conditions for plant growth, using mechanical (irrigation), chemical (fertilizer) and genetic (breeding) approaches to provide an environment that maximizes plant productivity.
What kinds of services can microbes provide?
The aspects of plant biology that microbes affect are comprehensive and take many forms. At any given time, microbial activities may be more or less important for each of these functions, but particularly under conditions of scarcity or stress, microbes are likely to be crucial to plant survival via one or more of the mechanisms described below.
Acquisition of nutrients
In addition to water, plants need nitrogen, phosphorous, potassium, sulfur, iron and other trace elements. Acquiring them is an ongoing challenge for plants and microbes are active participants in most of these processes. Indeed, bacteria are the only known organisms that can transform gaseous nitrogen into an organic form, ammonia, that can be used by plants. Prior to the development of industrial means to fix nitrogen, plants were entirely dependent on microbes for usable nitrogen. Both fungi and bacteria can help plants obtain adequate phosphorous.
Optimization of soil microbial communities could allow farmers to apply less chemical fertilizer, thus saving money and reducing the amount of excess nutrients that leach out of fields into water systems.
Other nutrients, like sulfur, potassium and iron can also be transformed into usable forms or transported to plants by both bacteria and fungi. Plants are subject to many potential biological enemies, including bacterial, fungal and viral pathogens that cause disease as well as parasites, insects, birds, and grazing animals that feed on plants. Partnerships with microbes can help plants resist these threats. In the simplest case, microbial partners may simply occupy niches that otherwise might be vulnerable to pathogens. When bacteria form a biofilm around the roots of a plant, microbial pathogens and soil–dwelling parasites cannot gain access. The beneficial microbes in the rhizosphere may be doing more than just getting in the way; they may also be producing any one of a number of chemicals that act directly against pathogens.
Many of the antibiotics humans use to treat infections are derived from bacteria or fungi that produce them to kill or inhibit competing microbes. Other microbially-produced chemicals may serve to mask the presence of the plant from would be parasites or predators, attract beneficial organisms, or stimulate the plants’ immune system. Bacteriophage — viruses that infect bacteria — may kill pathogenic bacteria directly. There is even evidence that microbes can generate electrical fields that can attract or deter other microbes and soil invertebrates like nematodes.
Above ground as below, microbes can serve the plant simply by occupying space that otherwise might be an entry point for pathogens. Surface and endophytic microbes also make a variety of potentially helpful compounds including toxins that deter grazers, volatile compounds that alert neighboring plants to the presence of a threat, and small molecules that trigger protective responses like the closing of stomata. There is crosstalk between the “conversations” going on between plants and the microbial communities above and below ground; events in the soil can trigger responses in leaves and vice versa. For example, when tomato plants are attacked by the early blight fungus, their activated immune system produces stress signals that are perceived by fungi that live around the roots. Through their hyphae, the beneficial root fungi then transmit the stress signal to neighboring plants warning them to up-regulate their stress responses. Microbes produce a wide array of compounds that inhibit or kill competing microbes.
If a bacterium, virus or fungus can deter another microbe that is harmful to a plant, it may well be in the plant’s interests to provide the helpful microbe with shelter and nourishment. It is likely that many plant-microbe partnerships have evolved on this basis: the plant supplies carbohydrates to certain microbes in return for the deterrence of pathogens or predators or other benefits. It has been estimated that up to 30% of a plant’s primary production (that is, the amount of carbon the plant turns into organic matter through photosynthesis) actually leaves the plant as exudate into the soil; the microbes must be making a fairly substantial contribution to earn such a high investment of the plant’s resources.
Resisting environmental stress
If, as just noted, microbes can earn a living protecting plants from predators, it stands to reason that microbes might also benefit from helping the plant survive times of environmental stress. Indeed, microbes have been shown to be important partners in mitigating the effects of virtually every known environmental stress that can affect plants.
Scientists are still unraveling the many ways that plants can make use of microbial capabilities to make nutrients more available or deter pathogens. Perhaps even more surprising, discoveries are emerging from the realization that microbes play critical roles in plant development, physiology and metabolism. These roles often are carried out through microbial synthesis of biochemicals that mimic, amplify, inhibit, or modify the activities of plant hormones. Some seeds require bacteria to germinate. Other microbial compounds enhance root respiration or affect transpiration by modifying the activity of stomata. Microbes can even affect the flavor of food plants.
There is much more going on in a plant’s world than meets the eye. A complex but largely invisible ecosystem surrounds each plant that includes bacteria, fungi, viruses, and soil invertebrates with multiple, interwoven networks of predation, pathogenesis, cooperation and interdependency. There are multiple, lively chemical conversations going on under our feet, conversations that include some overlapping vocabulary and unambiguous signals, but also numerous efforts to encrypt, deceive, or eavesdrop. The conversations connect plant to plant, plant to microbe, plant to nematode, microbe to microbe, nematode to nematode and every other conceivable combination — with viruses potentially participating in multiple ways. The inhabitants of these ecosystems can listen in on some of each other’s conversations, interfere with others, impersonate one another, and amplify or dampen signals; a single chemical can mean different things to different organisms or at different times.
How do plants and microbes interact?
Bacteria produce a number of small molecules that serve as quorum sensors — that is signals that bacteria use to determine the density of the local bacterial community and how many of their own species are present. Bacteria integrate these signals to cue group behaviors like biofilm formation or toxin secretion.
Another way that the various microbial organisms living around plants can interact both with plants and with one another is through direct transfer of genetic material. Bacteria exchange plasmids with each other via the process of conjugation, and viruses shuttle genes from one organism to another on a regular basis. This capability has been exploited in biotechnology to transfer desirable genes into plants.
Another form of interaction is the transfer of proteins between organisms. Bacteria and fungi both produce proteins called effectors that they inject into plant cells. A great deal of interaction between plants and microbes uses the language of plant hormones. Microbes produce a number of plant hormones, and they also produce enzymes that alter plant hormone levels. In return, plants produce compounds to block or modify the bacterially produced plant hormones.
Biotechnology powerhouses: We are not used to considering the members of ecosystems that function at the microscopic scale. Their activities, though invisible, are essential to the overall functioning of the ecosystem.
The potential applications of beneficial microbes in agriculture seem boundless, but progress will require advances in basic understanding of plant-microbe interactions coupled to practical attention to the process of moving discoveries from the lab to the field, as well as technical, regulatory, marketing, and end-user education issues. An integrated approach to addressing these challenges — in other words, an approach that acknowledges the multi-faceted nature of the challenges — is most likely to succeed.
Evolutionarily optimized microbial communities also might allow crop plants to grow in poorer soil or under the less predictable climactic conditions that will accompany continued climate change.
The microbial context in which the ancestors of current crop plants evolved surely differed from that in which their descendants are currently grown. Understanding the partners with which each plant evolved is a highly promising target of intervention to improve crop productivity. It seems clear that plants are able to recruit local microbes for many functions, but it is possible that providing plants with microbial partners more closely related to those with which the plant evolved could allow a dramatic reduction in the artificial inputs — including chemical fertilizers, pesticides, and herbicides— that humans have employed to help plants grow in new environments.
Roots are doing a lot more than holding plants in place. The myriad interactions taking place among plant roots, their exudates, and the thousands of species of microbes in the soil are fundamental to plant health and productivity. They remain, however, to a large degree, a black box. Methods for studying these interactions on a molecular level and in real time and space, are essential in order to determine the optimal community for plant productivity and successfully optimize the soil microbiome in the field.
Achieving food security for a still-expanding global population is a large and complex challenge. Increasing agricultural productivity without increasing pressure on natural environments or consuming more fossil fuels is a goal that will require progress across many fronts. Sometimes, however, a great need and a new opportunity happen to coincide. All plants, in all environments, depend on microbes, and therefore, potentially all crops, no matter where they are grown, could benefit from optimization of their microbial partners. The time is right to enlist the capabilities of the microbial world to help solve a pressing human problem.