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‘Profound ignorance’: Microbes, a missing piece in the biodiversity puzzle

  • Researchers are certain that human activity has resulted in a decline in plant and animal species. But a huge unknown remains: what impacts have human actions —ranging from climate change, to ocean acidification, deforestation and land use change, nitrogen pollution, and more — had on the Earth’s microbes?
  • A new paper poses this significant question, and offers a troubling answer: Science suffers from “profound ignorance” about the ways in which microbial biodiversity is being influenced by rapid environmental changes now happening on our planet.
  • Researchers are supremely challenged by the microbial biodiversity question, finding it difficult to even define what a microbe species is, and uncertain how to effectively identify, analyze and track the behaviors of microbes on Earth —microorganisms estimated to be more numerous than stars in the known universe.
  • We do know microbes play crucial roles — helping grow our food, aiding in the sequestering and release of soil carbon, curing and causing disease, and more. One thing researchers do agree on: knowing how human activities are influencing the microbial world could be very important to the future of humanity and our planet.

Scientists are clear: the number of plant and animal species on Earth is declining. The climate crisis, habitat loss, pollution and the illegal wildlife trade are all pushing species toward extinction. Researchers especially worry that losing too much biodiversity could push the earth past a tipping point into irreversible change, and on into a new paradigm in which humanity and other life can’t survive.

Which partly explains humanity’s self-interest and urgency in understanding and maintaining global biodiversity. But there’s a catch: most of Earth’s biomass isn’t composed of plants and animals, but rather of microscopic organisms found almost everywhere — in soil, the upper atmosphere and deep ocean trenches. Microbes help us grow food on our farms and to process it in our gut; they give us diseases and help cure them.

An ominous question looms: how will climate change, along with other human-destabilized planetary boundaries — ocean acidification, deforestation and land use change, ozone depletion, nitrogen and plastics pollution, and maybe worse — alter the microbial world?

According to a new paper, “we have no idea” whether diversity among microbes is growing or shrinking, whether we could be walking blind toward microbial extinction cliffs — or soon be living in a world more dominated by microbes.

“We’re pretty clear that macro-biodiversity is in decline, but whether micro-biodiversity is going the same direction, we’re not sure,” says David Thaler, a microbiologist at the University of Basel and study author.

A microbial community on the human tongue. Each color represents a different type of microbe. The white material in the core represents the remnants of human tongue cells about which the microbes grow. Image courtesy of Steven Wilbert, Gary Borisy, Forsyth Institute; Jessica Mark Welch, Marine Biological Laboratory.

Into the microscopic darkness; asking the right questions

High biodiversity among plants and animals improves an environment’s resilience to sudden shocks and changes. The more species there are, the greater the chance that an ecosystem can bounce back after a destructive storm or intense drought, for example. As a result, scientists include biodiversity among the nine identified planetary boundaries, or environmental limits within which Earth’s current life support systems operate. But human activity, scientists say, threatens to rid the earth of many species irreversibly, and with them potentially the systems upon which humanity survives.

Microbes are hugely abundant, and that abundance, or lack of abundance, can affect multiple planetary boundaries. They, for example, take millions of tons of nutrients, such as nitrogen, out of the atmosphere every year and make that element available to other organisms, like plants, aiding in their growth. Of all the carbon removed from the atmosphere, microbes are responsible for 40% annually. Some scientists have called microbes “the most functionally important organisms on Earth,” and have recommended including microbes in climate policy research.

Microbes, by far, also carry most of Earth’s genetic material. If the genes of biodiversity were like a library, the shelves occupied by microbes would dwarf all others. Accessing that library has given scientists tools to better understand the world and address other medical and food challenges. For example, the most common COVID-19 test today uses enzymes originally sourced from microbes in hot springs.

Thaler asks: “Is the whole library getting bigger or smaller? And are the macrobes — the humans — becoming a bigger or smaller part of that library?”

That question sharply differentiates between the biodiversity humans can and can’t see with the naked eye, and raises more big questions. Microbes perform core roles in ecosystems, but is microbial biodiversity necessary for those roles? And if so, which roles? How would a scientist measure microbial biodiversity in the first place? And how might human activity be impacting microscopic abundance and diversity and where?

Technology to understand microbes, while constantly improving, is still unable to easily identify the diversity of microbial species — even in a 0.5 gram soil sample. Scientists estimate that only between 1% to 10% of microbes have been classified, allowing them to be cultured in a lab and studied further. Thaler’s question can’t be answered with current technology; instead, he’s interested, at the moment, in simply framing the right question.

“I’m interested in knowing the trajectory of biological information as a whole,” Thaler says. “To me it seems like the ‘path with heart,’ to try to understand whether the microbial diversities are increasing or decreasing, and to understand the question better, because it is probably the majority of biological information that we live within.”

‘Profound ignorance’: Microbes, a missing piece in the biodiversity puzzle
Microbial community on the surface of kelp. Each dot or filament is a bacterial cell and the different colors indicate different kinds of bacteria. The larger, ridged ovals are single-celled algae called diatoms. Image courtesy of Tabita Ramirez-Puebla and Jessica Mark Welch, Marine Biological Laboratory.

Microbes more countless than stars

Microbial diversity is already known to be immense and much greater than plant and animal diversity. There may be one trillion different microbe species on Earth, and individual microbes may number one million trillion times that. That’s ten million times the number of stars in the known universe. There could be half a million different types of microbes in just a liter of seawater, according to research by microbiologist Mitch Sogin.

“Then what does all that mean? Why does nature design that system so we have lots of rare taxa accounting for lots of diversity? Why does nature need all that diversity? What is the advantage?” asks Sogin, who is based at the Marine Biological Laboratory in Massachusetts.

Maggie Yuan, a microbiologist at the University of California, Berkeley, sees microbial diversity as a fundamental issue in ecology. Diversity, she says, can determine what nutrients soil can provide to crops, and whether, or how, the floods and droughts of climate change will affect agriculture.

“Understanding the diversity, or change in diversity, is relevant to many other topics. For example, how stable the diversity is and what ecosystem functions this diversity can perform,” says Yuan. However, “all these questions are depending on how we assess diversity, and now we are not even sure what overall diversity is.”

Scientific definitions of microbial biodiversity vary widely, and researchers note that the advantages of biodiversity seen in large plants and animals may not even apply to their microbial neighbors. Conventional biodiversity, for example, draws boundaries between species, making it easier to quantify and design conservation programs. But on a micro-level, it’s more difficult to draw those lines, unless they’re in sand.

Biodiversity under a microscope needs a different framing, says Sogin. To him, it doesn’t make sense to speak about “species” of microbes, but rather more simply “kinds.” Yuan has classified microbes into groups using calculations based on their relationships. How close is close enough to be the same microbial species, she asks? Some microbiologists say species can be defined by 97% similarity in some genes. However, when comparing that micro threshold with a macro equivalent, “then you can say human and mouse are the same species,” Yuan says.

‘Profound ignorance’: Microbes, a missing piece in the biodiversity puzzle
Another microbial community on the surface of kelp. Each dot or filament is a bacterial cell and the different colors indicate different kinds of bacteria. The larger, ridged ovals are single-celled algae called diatoms. Image courtesy of Tabita Ramirez-Puebla and Jessica Mark Welch, Marine Biological Laboratory.

Infinite riddles, wrapped in mysteries, inside enigmas

As researchers seek to define microbial biodiversity, the field becomes a battleground upon which our standard scientific thinking about evolution is often shattered. Are there really species? Are they separate from individual organisms (think, human gut flora)? Can “species” exchange DNA to become something new?

The microscopic world is detached from human experience, and scientists typically have relied on analogies to understand it. Information in microbial genomes are like “libraries,” “banks,” or an “expanding universe,” and their evolution is like a “tangled tree” or as Thaler says, disparate stars and galaxies.

Microbes tangle their evolutionary tree because they don’t always share genes or create new genetic material by conventional sex. For example, microbes can exchange DNA by way of contact with other transmitters or through viruses. If large plants and animals “vertically” create the tree of life in offspring, microbes can also use these mechanisms to “horizontally” share genes and bud new life.

Genetic variation comes when those mechanisms to create new life are imperfect and allow for mutation. Because generation times are so much shorter, microbes can mutate and go extinct, or multiply, orders of magnitude faster than humans or other life visible to the naked eye. In a Harvard medical experiment, bacteria were able to mutate so they could evolve to withstand antibiotics that were originally 1,000 times their tolerable limit — in just 11 days. How then, might climate change, with its surging temperatures, melting icecaps, devastating droughts and storms, alter the microbial world? The mind boggles.

Overwhelmed by these complexities, current technology can’t answer Thaler’s question. Deciphering data requires years just to determine the genomic codes from microbes held in a mere half gram of soil. Even then, scientists can only guess that they haven’t missed variants upon variants.

One method to measure diversity, Thaler says, is to gauge the potential of a sample to create new genomes. Alternatively, scientists can measure the parts of microbes that are directly valuable to humans: the parts of microbial genomes that allow them to perform functions like decomposition or carbon sequestration. Yuan doesn’t think there’s a study yet that can claim to have captured all the diversity in a single sample, especially in soil.

“Based on where we are at, based on where human research is at, it’s impossible,” says Yuan.

‘Profound ignorance’: Microbes, a missing piece in the biodiversity puzzle
Different microbial soil characteristics appear in different depths of a soil core: These soils contained very different compositions of microorganisms, even if they were collected at locations just centimeters away from each other. The CiPEHR field experiment in Alaska is operated by Dr. Edward Schuur’s research group at Northern Arizona University. Image courtesy of Maggie Yuan.

To conserve or not to conserve

As scientists learn more about microbial diversity, their research informs work to protect ecosystems. However, much conservation work to date has overlooked the status of microbes in ecosystems.

“There is no agency yet monitoring the state of the microbial world, and no World Wildlife Fund, no Nature Conservancy for microbes. Perhaps one day soon we will realize and rectify our neglect and lift our respect for the diversity of microbial life,” says Jesse Ausubel of the Rockefeller University’s Program for the Human Environment, a sponsor on Thaler’s study.

It is known that some microbes performing key roles in soils and earth systems have come under threat due to human activity. Overused soils, for example, have depleted nutrients and less abundant microbes, while overfishing and ocean acidification threaten the microbes that maintain coral reefs and sequester carbon at the bottom of the ocean. Even in the human gut microbiome, activities like urbanization, food standardization and improved hygiene have led to a decline in microbes that long helped humans process food and fight disease.

Microbes have changed in the face of anthropogenic change, potentially exacerbating processes that are bringing the earth closer to its planetary boundaries. Yuan at Berkeley recently published results that suggest microbes may thrive in a warming climate. In slightly higher temperatures, microorganisms in soil were shown to build more connections with other types of microbes. Those new interactions may engender greater diversity, or lead to worse outcomes for humans. For example, a warming tundra may release millions more microbes to decompose organic material and release methane — a hugely powerful greenhouse gas.

‘Profound ignorance’: Microbes, a missing piece in the biodiversity puzzle
KAEFS global change field experimental plots, in Oklahoma, managed by Dr. Jizhong Zhou’s research group from the Institute for Environmental Genomics at the University of Oklahoma. Above and inside the plots are infrastructure and equipment that introduce ecosystem warming and precipitation alterations. Soil samples are collected regularly from these plots to study how climate change might affect belowground microbial communities. Image courtesy of Maggie Yuan.

In agriculture, microbial conservation focuses on healthy soils as measured by nutrient content. By encouraging nutrients, associated microbes that cycle those nutrients in and out of plants will have an easier time performing the roles useful to food production. Also, microbes generally have high “functional redundancy,” says Yuan, meaning that many microorganisms perform the same functions. If one disappears, others will likely be able to fill in the gap and continue cycling nutrients.

“For example, when it’s warmer or drier, do we have some microbes that come and help the plants deal with the drought or the heat?” asks Yuan. “With functional redundancy being higher, the whole system should be more stable because if one species goes extinct, other species can perform a similar function.”

However, observing these microbiome changes is challenging: microbes can go extinct and evolve into completely different ecosystems faster than scientists can identify and measure them. For instance, if soils or aquifers get polluted, microbes may be killed, but new ones that survive in extreme environments may also evolve. How do we identify and track the microorganisms in this evolving system, and how do we know which kind of microbe we should conserve?

“Whether higher [microbial] biodiversity is better for microorganisms, I don’t think people have consensus on it,” says Yuan. “First of all, if we talk about losing diversity, how low is really low? It can be high, but how high can become a problem? The answer depends on the system under discussion, and we don’t know yet on a global scale.”

‘Profound ignorance’: Microbes, a missing piece in the biodiversity puzzle
Soil samples collected from the KAEFS global change field experiment. These samples are archived at -80 degree Celsius to preserve microbial DNA and RNA materials. Microorganisms found in soils from warming vs. ambient temperature treatments, or those in soils collected in different years or seasons, show very different compositions. Image courtesy of Maggie Yuan.

Microbial diversity, rather than itself being a target of conservation, could also be integrated into conservation programs as warning signals, alerting us before macro species are put on the brink. Sogin believes that drastic ecosystem change may first show up in microbe populations, whether in water, bodies, or soils.

“By looking at how those microbiomes shift, it might be predicted how those host animals may be threatened by extinction,” says Sogin. “The way you are able to determine whether your mitigation efforts are productive or will be productive would be to see if it mitigates the shifts in the microbiosphere first.”

Thaler recognizes that determining the status of microbial diversity around the world is unknowable, at least for the next twenty years. “So, this is really about framing the right question,” he says, and then questing for answers.

Citations:

Thaler DS (2021) Is Global Microbial Biodiversity Increasing, Decreasing, or Staying the Same? Front. Ecol. Evol. 9:565649. doi: 10.3389/fevo.2021.565649

Cockell, C., & Jones, H. (2009). Advancing the case for microbial conservation. Oryx, 43(4), 520-526. doi:10.1017/S0030605309990111

Shoemaker, W., Locey, K. & Lennon, J. A macroecological theory of microbial biodiversity. Nat Ecol Evol 1, 0107 (2017). https://doi.org/10.1038/s41559-017-0107

Finlay BB, Amato KR, Azad M, Blaser MJ, Bosch TCG, Chu H, Dominguez-Bello MG, Ehrlich SD, Elinav E, Geva-Zatorsky N, Gros P, Guillemin K, Keck F, Korem T, McFall-Ngai MJ, Melby MK, Nichter M, Pettersson S, Poinar H, Rees T, Tropini C, Zhao L, Giles-Vernick T. The hygiene hypothesis, the COVID pandemic, and consequences for the human microbiome. Proc Natl Acad Sci U S A. 2021 Feb 9;118(6):e2010217118. doi: 10.1073/pnas.2010217118. Erratum in: Proc Natl Acad Sci U S A. 2021 Mar 16;118(11): PMID: 33472859; PMCID: PMC8017729.

Locey, K. J., & Lennon, J. T. (2016). Scaling laws predict global microbial diversity. Proceedings of the National Academy of Sciences, 113(21), 5970-5975. doi:10.1073/pnas.1521291113

Yuan, M.M., Guo, X., Wu, L. et al. Climate warming enhances microbial network complexity and stability. Nat. Clim. Chang. 11, 343–348 (2021). https://doi.org/10.1038/s41558-021-00989-9

Cavicchioli, R., Ripple, W.J., Timmis, K.N. et al. Scientists’ warning to humanity: microorganisms and climate change. Nat Rev Microbiol 17, 569–586 (2019). https://doi.org/10.1038/s41579-019-0222-5

Banner image: Each animal is a microcosmos on its own. This scanning electron micrograph shows diverse microorganisms on the leg of a water bug (Ranatra fusca). Diatoms (cyan) intertwined with bacteria (purple) and unknown filaments that may be alive (yellow). Colors were added manually. Image courtesy of Emil Ruff, Kristina Garcia.

Animals, Biodiversity, Biodiversity Crisis, Biodiversity Hotspots, Carbon Sequestration, Climate Change, Climate Change And Biodiversity, Climate Change And Conservation, Climate Change And Extinction, Climate Science, Conservation, Earth Science, Ecosystems, Extinction, Forgotten Species, Green, Microorganisms, Plants, Research, Saving Species From Extinction

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