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Intensive agriculture changes the soil microbiome

California rice fields are a living laboratory of plant-driven change to the soil microbiome. Image credit: C. Santosh Kumar, UC Davis

California rice fields are a living laboratory of plant-driven soil microbiome changes. Image credit: C. Santosh Kumar, UC Davis

California rice farms dot the Sacramento Valley, converting native swampland into flooded paddies. The farms change California’s landscape both above ground and below it. A recent study shows in detail how rice plants shape the soil microbiome into a distinctive mix of bacteria and archaea, which become widespread as farmers grow the same crop year after year.

“Intensive rice cultivation domesticates the soil,” says coauthor and University of California, Davis plant biologist Venkatesan Sundaresan, summing up the recent findings. Sundaresan and his colleagues also showed, based on experimental evidence, that the soil changes affect rice crop yields over time.

The idea that plants shape the cocktail of bacteria, archaea, and other microbes attracted to their roots is decades old. The concept of “soil fatigue,” for example, comes from observations of plants attracting soil pathogens that become more abundant over successive growing seasons of the same crop. Eventually agricultural productivity falls, explains microbial ecologist Alexandre Jousset at Utrecht University in the Netherlands.

What sets this recent work apart, he says, is its unusually thorough methodology, which extends beyond the standard observation and correlation of plants and certain microbes, to experimental evidence that plants drive soil microbiome changes.

First Sundaresan and collaborators collected soil samples from monocrop rice fields at three different Northern California farms. The researchers also collected soil from uncultivated grassy patches, which they called “wild” soil, at two sites next to rice fields.

Back at the UC Davis greenhouse, the researchers grew sterile rice seedlings potted in each type of soil. They also had control flower pots, with each type of soil, but no seedlings. What they found was that initially, rice grown in cultivated soil attracted more Acidobacteria, Deltaproteobacteria, and Euryarchaeota archaea, among other taxa, compared to rice in wild soil. And over time, the microbial community around rice roots in cultivated soil continued to resemble the community in control pots that contained cultivated soil only.

However, when they ran the same experiments with wild soil, bacteria in flower pots with seedlings did not resemble bacteria in flower pots with soil alone over time. It appeared that the rice was changing the soil, to resemble the cultivated field. Though the wild soil didn’t become identical to cultivated soil in a single rice generation, “it was trending in that direction,” Sundaresan says.

To determine whether plants besides rice can drive the observed changes, the researchers grew weeds in both wild and cultivated soils. The weeds also changed the soil, but attracted different microbial communities than the rice plants.

The soil changes don’t necessarily benefit the rice, however, even though the rice is manipulating the soil. Contrary to Sundaresan’s expectations, rice seedlings grown in sterile clay, and inoculated with microbes from either kind of soil, grew faster with microbes from wild soils, and slower with microbes from cultivated soils. Filtering out the microbes prevented reduced growth.

But intriguingly, when the researchers grew seedlings in clay inoculated with microbes from a monoculture field left fallow for several years before the experiment, the seedlings grew faster than in any other soil treatment. That implies monocultures could have beneficial microbes as well as growth-limiting ones. That “was probably the coolest part” of the study, says microbial ecologist and plant pathologist Linda Kinkel at the University of Minnesota in Saint Paul.

Previous work has shown that monocultures can shape the microbiome to a farmer’s benefit. For example, repeated planting of wheat builds up antibiotic pseudomonas populations in the soil that suppress certain pathogens, she says. This latest study only sampled one fallow field, which is insufficient to draw major conclusions, but invites follow-up study, Kinkel notes. It’s possible that both beneficial and harmful microbes build up in monoculture soils, she says, but that the detrimental strains die out faster, leaving the good ones in rested fields.

“The takeaway,” Sundaresan says, “is that crop cultivation is changing the soil microbiome.” And apparently it’s doing so with mixed consequences for plant growth. A logical next step, he says, is figuring out how to manipulate the soil community to benefit crop yields.

Similar efforts are already underway to manipulate the soil microbiome for disease resistance, says Britt Koskella, a disease ecologist at the University of California, Berkeley. An explosion of recent research, she says, uses successional planting of different species to create healthy, disease-resistant soil microbiomes. A 2018 study for example, found that fields planted with five rotating crop species were 9% better at suppressing disease than monoculture fields. “That’s pretty striking,” Koskella says.

Though Koskella disagrees with Sundaresan’s use of the term “domesticated” in the context of rice-altered soil, she lauded the study as a worthy addition to a growing literature on interactions among plants, soil, and the microbiome. “All of this has to do, in the end, with how we use microbes to benefit crop breeding,” Sundaresan says.

Categories: Agriculture | Microbiology and tagged | | | |
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