Functional Redundancy (Part 2): Macroscopic Lessons at the Micro Scale

This is part of our sequence of blogs about “functional redundancy”, a concept from ecology that explains why diverse ecosystems are often more productive and resilient. The following series explores this history of the concept of functional redundancy, why it matters to agriculture, and how we can use it to build better biological products that function consistently across environments.

The black box open

For most of the history of ecology, microbes were a black box. Researchers knew soil microbes cycled nutrients and decomposed organic matter, but most aren’t easily grown in a lab, so there was no practical way to see who was actually there. Plant and animal ecologists could count species in a plot. Microbiologists largely couldn't.

DNA sequencing changed this. Once researchers could read genetic material in soil, water, and roots, they discovered communities of staggering diversity: thousands of organisms in a pinch of soil. The same questions from macroecology followed immediately. If there are this many species of microbes, how many of them are doing the same jobs? Does all this diversity actually matter for function?

Carrying macroecology underground

Microbial ecology inherited its framework from macroecology, but microbes force some rethinking. An influential 2008 review by Allison and Martiny looked at whether microbial communities were resistant, resilient, or functionally redundant under four kinds of disturbance.

The answer was sobering for anyone who assumed microbes were insensitive to disturbance. Many did not bounce back right away, regardless of the type of disturbance or how broadly the group was defined. Other studies showed that shifts in microbial composition often came with changes in the rates of ecosystem processes. In plain terms: when you disturb a soil community, it changes, and those changes alter what the soil is capable of doing (for plants).

A decade later, Louca and colleagues looked at the other side of the coin. They noted microbial communities can look wildly different from one sample to the next in terms of who is there, while the overall jobs being done stay remarkably similar indicating functional redundancy is a key metric for microbial ecosystems.

Why microbial redundancy is complex

Several features of microbial life make redundancy both more common and harder to pin down than it is for microorganisms like plants and animals:

• Genes move sideways. Bacteria can pass genes directly to unrelated neighbors, so a useful capability can spread across very different organisms.
• Dormancy is a strategy. Many soil microbes can go dormant when conditions turn against them and wake up when favorable. A soil can hold a "seed bank" of backup workers that only perform a function when activated.
• Numbers are enormous. Huge populations and fast generation times mean that both the composition and function of communities can shift quickly, for better or worse.

There's also a measurement caveat that runs through all of this. High functional redundancy with microbes can mean that function was categorized too coarsely. For example, If you define the job as "cycles nitrogen," many organisms qualify. Define it as "converts ammonium to nitrite in cold, acidic soil," and the list gets much shorter. Making sure multiple mechanisms are in place for doing the same function means considering how, when or where they do it best.

Health, imbalance, and the question of "invasion"

To see why this matters, it helps to look at what happens when a system loses its balance. The parallels between large-scale ecosystems and microbial ones are striking.

At the macro scale. Consider species labeled "invasive," like kudzu in the American Southeast or cheatgrass in the West. We put "invasive" in quotes here deliberately. Whether an organism becomes a problem usually depends less on what it is than on where it is. Cheatgrass isn't a villain in its native range but becomes one where disturbance has opened space, the native competitors that would hold it in check are missing, and its life cycle happens to fit the local fire and moisture patterns. The same is true of microbes: whether one is harmless, helpful, or a pathogen is often a matter of context, companions, and environment. (This idea deserves its own post, and it will get one.) Takeover tends to happen when ecological niches are open, when the organisms that would normally compete for those resources are absent or weakened.

At the micro scale. The human gut offers another familiar version of this story. A course of broad-spectrum antibiotics can knock back the resident gut community, and Clostridioides difficile, a bacterium that lives in a great number or us humans quietly, can then grow out of control. The organism didn't change. The community around it did.

This occurrence is also well-documented in disease-suppressive soils. Disease-suppressive soils are soils where crops show little or no disease, even though a soilborne pathogen is present or disease had appeared in previous years. Protection comes from other, free-living or non-pathogenic soil microorganisms that keep the infection (or population) levels of the pathogen in check. In a 2011 study of sugar beet, Mendes and colleagues detected more than 33,000 bacterial and archaeal species in the root zone and identified key groups associated with suppressing a fungal root pathogen. They concluded that when pathogens attack, plants draw on microbial consortia for protection. The protection came from a community, not a single hero organism. A lesson that growers who maintain diverse, healthy soils have learned the benefits of well.

A 2015 experiment went a step further and asked what, exactly, it is about a community that resists invasion. Wei and colleagues tested how the resource-competition networks of resident root bacteria affected invasion by the tomato wilt pathogen Ralstonia solanacearum, and found communities that overlapped with the pathogen in the resources they used limited pathogen growth, and produced fewer diseased plants in greenhouse tests effectively starving out the R. solanacearum.

The point is that it wasn't just how many species were present. It was how they fit together: whether the community collectively filled the niches the pathogen needed.

The shared lesson

Across plant ecosystems (kudzu, cheatgrass), the human gut (C. difficile), and our crop’s rhizospheres (root pathogens) the lesson is the same: health is less about the absence of bad actors and more about a community with enough filled functional niches, and enough backup for those niches, that bad actors can't take over.

That's functional redundancy and response diversity doing their job. So how do we get this benefit into the field? 

References

• Fiegna, F. et al. (2015). Evolution of species interactions determines microbial community productivity in new environments. The ISME Journal 9: 1235–1245.

• Tsiafouli, M. A. et al. (2015). Intensive agriculture reduces soil biodiversity across Europe. Global Change Biology 21: 973–985.

• Wei, Z. et al. (2015). Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nature Communications 6: 8413.

• (2022). Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community. The ISME Journal.

• Ehrlich, P. & Ehrlich, A. (1981). Extinction: The Causes and Consequences of the Disappearance of Species. Random House.

• Elmqvist, T. et al. (2003). Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the Environment 1: 488–494.

• May, R. M. (1973). Stability and Complexity in Model Ecosystems. Princeton University Press. Tilman, D. & Downing, J. A. (1994). Biodiversity and stability in grasslands. Nature 367: 363–365.

• Walker, B. H. (1992). Biodiversity and ecological redundancy. Conservation Biology 6: 18–23.

• Yachi, S. & Loreau, M. (1999). Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. PNAS 96: 1463–1468.

• Allison, S. D. & Martiny, J. B. H. (2008). Resistance, resilience, and redundancy in microbial communities. PNAS 105 (Suppl. 1): 11512–11519.

• Louca, S. et al. (2018). Function and functional redundancy in microbial systems. Nature Ecology & Evolution 2: 936–943.

• Mendes, R. et al. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332: 1097–1100.

• Wei, Z. et al. (2015). Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nature Communications 6: 8413.