Can microbiome adaptations protect crops from pests and climate change?

Kevin Hockett is an avid sourdough baker. As a microbial ecologist at Pennsylvania State University in University Park, he knows that each of his perfectly risen loaves is, in large part, the result of a living community of yeast and bacteria in the sourdough starter. Every time he reserves some successful starter to add to a future batch, he is selecting for a community of microbes that is well suited to making good bread.

So, when Hockett came across a 2015 review paper suggesting that microbial communities might be adapted over time to improve crops, the concept immediately resonated with him (1) and sent his research in a new direction that may one day lead to a valuable new tool for supporting crops.

For millennia, growers have improved agriculture by directing the evolution of crops themselves—only carrying on seeds from plants that survived disease, grew the fastest, or made the largest fruits. But as climate change rapidly alters growing conditions and the spread of disease, it’s becoming more difficult for the slow work of these conventional breeding approaches to keep up. Using genetic engineering to modify crops can help, but it, too, is time-intensive because researchers must first identify the beneficial genes, notes Hockett. And even after a resistance gene is introduced into new cultivars, pathogens can evolve to dodge its effects.

“Breeding will still have its place in the toolbox,” Hockett says. But, he adds, “the microbiome approach will likely be far quicker.” Already, these approaches are showing promise as a way to nurture better, more resilient crops. But researchers are struggling to devise the microbial combinations that will have real, lasting effects.

Group Effort

Plants depend on their microbiomes for many services—from capturing nutrients to fighting off pests. Just as the microbial community in a sourdough starter could be selected over time to produce a crisper crust, perhaps, Hockett thought, the microbial community surrounding a plant’s roots or leaves could be pushed toward supporting a healthier plant. The review paper that Hockett discovered mentioned only a few studies that had successfully attempted this feat, and largely with a model plant rather than crops (1). But Hockett and his then-graduate student, microbial ecologist and plant pathologist Hanareia Ehau-Taumaunu, decided to try, nonetheless.

In 2019, they attempted to coax a tomato microbiome to make the crop more disease-tolerant. Ehau-Taumaunu sprayed more than 70 tomato seedlings with a microbial brew collected from the leaves of healthy, field-grown tomatoes. She then sprayed the seedlings with Pseudomonas syringae pv. tomato, a problematic bacterial pathogen for Pennsylvania tomato growers that causes yellow-rimmed dark spots on infected leaves, indicative of a disease known as bacterial speck. After about a week, she collected leaves from the most well-protected plants—those with the smallest leaf area covered in spots. Ehau-Taumaunu then harvested the microbiomes from these leaves to spray onto the next planting of seedlings.

By repeating this again and again, she kept the tomato seedlings genetically identical, only selecting the most beneficial microbial communities to carry on to the next planting. For each of the first seven rounds of this process, known as passaging, the selected microbiome didn’t seem to offer any more protection than in the previous round. But at round eight, disease prevalence suddenly dropped. “It gave me hope that this might work,” says Ehau-Taumaunu, now a joint postdoctoral fellow at the New Zealand Institute for Plant and Food Research in Auckland and Bioprotection Aotearoa in Canterbury.

Spurred on by early successes, Hockett’s team and a select group of microbiologists across the world continue to passage microbiomes in pursuit of better crops. They’ve shown, for example, that passaged microbiomes not only reduce tomato infection (2), but can speed mushroom development (3) and increase mung bean salinity tolerance (4).

Passaging doesn’t always work, however (5)—and when it does, it’s often unclear which combinations of myriad microbes are responsible, or how that community could be transferred to a grower’s field. But many of the researchers set on steering crop microbiomes toward their most beneficial potential feel that these hurdles are surmountable. Passaging, Hockett says, “is an untapped tool.”

The Whole Community

Academics and farmers have long understood that microbes can benefit crops. For over a century, growers have inoculated fields with rhizobia—bacteria that colonize legume roots and convert nitrogen from the atmosphere into a form that plants can access. In more recent decades, growers have actively managed fields to encourage arbuscular mycorrhizal fungi, which help plants take in a range of nutrients. And they’ve defended crops with Bacillus thuringiensis, a bacterium that produces toxins that kill pests.

But typically, these and other microbial applications rely on a single microbe at a time (6). Only in the past decade have academics and the agricultural industry started to explore whether communities of microbes might give crops a better boost, explains microbial ecologist Janet Jansson, an emeritus chief scientist at the Pacific Northwest National Laboratory in Richland, Washington. “If you have a consortium of microorganisms, you may be able to increase the number of functions that the community can carry out,” she says. Researchers theorize that diverse community members might also support one another, making it easier to survive on a plant’s leaves or roots and compete with existing microbial communities in fields (6).

Some microbial ecologists culture and combine individual beneficial strains (6). Others, like Hockett, collect whole interconnected communities of bacteria, fungi, viruses, archaea, and protozoa from foliage or soil surrounding roots. When these researchers then passage a natural community, they shape its membership. Strains that offer no benefit to a target trait can be whittled away with each passaging round, while individual strains may also evolve to become even more beneficial to the plant (1). A plant can also play an active role in this process by releasing sugars, amino acids, and other molecules that encourage beneficial microbes to proliferate.

In 2020, Hockett and Ehau-Taumaunu passaged the tomato leaf microbiome again to confirm their results. In this larger study, disease severity steadily increased during the first few passages, but declined after the sixth passage when the microbial community adapted to suppress bacterial speck. The selected microbiome offered progressively greater protection through the next several passages (2). By the ninth and final passage, bacterial speck was 20–30% less severe than at its peak earlier in the experiment.

Hockett doesn’t know how this passaged microbial community suppresses disease, so he’s sequencing the microbiome from different passaging stages to find out. His preliminary results, not yet published, suggest that the community shifted to include more bacteria that could outcompete the pathogen for key nutrients. In the future, Hockett hopes to develop these communities in the greenhouse and provide them to farmers to deploy in the field.

Microbiome Wins

Directing the adaptation of crop microbiomes can do much more than improve pest resistance, and researchers are already using it to address a host of other agricultural challenges.

In 2022, Hockett used passaging to accelerate a mushroom’s life cycle to increase production (3). Pennsylvania growers, who lead the nation in mushroom production, grow crop after crop continuously indoors. “If they can speed up the development, they can go through more production in a given year,” Hockett explains. His team cultivated button mushroom spores and watched for “pins,” the tiny fruiting bodies that develop into mushrooms. Then, they collected a matting of peat moss mixture—along with its microbiome—from below the pins that formed the fastest. They used this planting material to grow the next crop. After only three rounds of passaging, his team had a microbiome that could speed up pinning by three to four days. That’s not enough for a meaningful increase in annual yields, but it gives Hockett hope that, with more passaging rounds, he can speed mushroom development even further. He’s also now testing how selecting the microbiome for shortened development time could help mushrooms outcompete pathogens like green mold for the same growing space.

Among climate change’s inauspicious effects are spikes in salinity in some parts of the world—a big problem for many crops. At the Indian Institute of Technology Delhi, environmental microbiologist Shilpi Sharma is shaping microbiomes to buffer plants from soil salinity. Climate change is increasing salt levels in soil through many routes, including rising ocean levels and decreasing rainfall (7). “By 2050, it is believed that India will lose 50% of its arable land to salinity,” Sharma says (8).

In 2017, Sharma’s team grew mung bean—a staple in many Asian diets—in pots containing a mixture of soil from ecosystems across India. They adjusted the salt level to 150 millimolar, making it far saltier than typical soil on Indian farms. Within five passages of root microbiomes collected from the healthiest plants, the team had a microbiome that could help plants survive this salt stress (4). They then began ramping up the salt content every other passage until they reached 180 millimolar at the 13th passage. “We didn’t want to stop,” Sharma says. “We just wanted to see where the end is.” Ultimately, her team’s passaged microbiome supported plants that thrived at this high salinity level—weighing over twice as much as mung bean plants grown in this same soil type without the aid of the artificially selected microbial community (9).

Passaging can also improve the mineral content in soils. Microbial ecologist Eiko Kuramae of the Netherlands Institute of Ecology in Wageningen and Utrecht University in Utrecht recently passaged microbiomes to select for a microbial community that excels at transforming phosphorus into a form that plants can take up (10). “A significant portion of applied phosphate fertilizer becomes immobilized in the soil, rendering it unavailable to plants,” Kuramae says. “Phosphate-solubilizing microbes can release this fixed phosphorus, reducing the reliance on conventional fertilizers.” That could ultimately reduce the pollution of waterways caused by the runoff of excess fertilizer, for example.

The team started by extracting the microbiome from a grassland soil collected in the Netherlands. Back in the lab, they seeded different combinations and concentrations of these starter microbes into a liquid growing medium, which contained phosphate in a form that plants couldn’t access. Unlike many other passaging studies, they used nutrient levels in this growing medium—rather than the health of a crop—to determine which microbiomes to select for the next round of passaging. Every few days, they tested which growing media contained the most plant-accessible phosphorus and then used the microbiomes from those containers to seed more growing media. After seven rounds of passaging, the artificially selected microbiome unlocked nearly 25% more phosphorus for plants than the initial microbiome used to start the experiment.

From Lab to Field

Despite these early wins, passaging is not a cure-all. In many cases, even in a controlled lab setting, it simply doesn’t work—often for reasons that aren’t clear (5). Microbiome scientist Laramy Enders of Purdue University in West Lafayette, Indiana, recently made several attempts to artificially select a tomato root microbiome to reduce the crop’s susceptibility to pests. Passaging had no effect on fending off caterpillars (5).

Passaging did ramp up protection from aphids, but only briefly; the microbial community often lost its protective power from one passage to the next, only to regain it at a later passage (5). Enders suspects that the three-week period between seed planting and aphid introduction allowed too much time for the microbiome to continue changing without pressure from the pest. This finding suggests that growers will need to carefully time microbiome applications, Enders says. “You might want to wait until later in the season, when you expect there to be more aphids present,” she says, “because the stability of that community may only be short term.”

For passaged microbiomes that do support crops, there are many ways in which growers could apply them, including seed coatings, sprays, and irrigation additives (11). “The major bottleneck is the process to store it,” Sharma says. Many of the potentially beneficial species in a passaged microbiome can’t be grown in a lab. So, Sharma and others are studying how best to freeze whole communities so that they can survive in a freezer and later be applied to a field. Currently, many strains lose their beneficial effects after thawing, she says.

Kuramae thinks that microbial ecologists could also develop protocols that allow farmers to sample and then passage their own microbial communities. “Starting with the microbial community in their soil would increase the likelihood of the selected community being compatible with the native soil microbiome,” she explains.

The Right Recruits

In the meantime, Sharma and others are sequencing microbiomes at different stages of passaging to identify individual community members and how their numbers correlate with benefits to the plant (9, 12). Microbial ecologists could then create new communities with a subset of the most beneficial members that can be cultured in the lab. Using this approach, Sharma already created a microbial community of bacteria that she coated onto mung bean seeds to increase salinity tolerance in a field experiment. According to Sharma, the unpublished results from the work suggest that this subset of the microbiome was just as effective at supporting the crop as the complete passaged microbiome.

For now, it’s unclear whether the passaged microbiome—either whole or downsized to a select few—will prove more effective than simply combining microbes that are already known to benefit crops.

Hockett acknowledges that the process of passaging an entire microbial community can be highly variable. Environmental factors, such as temperature and moisture, as well as management practices like fertilizer applications, can all affect microbial communities. Each time his team collects a leaf from a field and begins passaging its microbiome, the starting community is unique. This natural variability, he believes, is one reason why selecting for a protective tomato microbiome required eight passages in his first attempt and only around six in his second.

In contrast, communities built from a few, easily cultured microbes are far simpler to reproduce. Yet, they may also be missing potentially powerful plant helpers that are only revealed through passaging. For now, Hockett’s motivated by a central hunch: “the more diversity we start with, the more potential solutions we’ll find.”