Why Aren’t Subseafloor Microbes Cleaning Their Plates?

A new review article discusses the role of subseafloor microbes in driving global biogeochemical cycles. The authors propose a new explanation for why microbes fail to consume all the organic matter available to them, a state of affairs that has caused the surface world to become more oxidized over time.

From their humble location deep in the muck at the bottom of the ocean, subseafloor microbes unknowingly pull the levers that control Earth’s biogeochemical cycles. The speed that they consume carbon, oxygen, sulfur, and other elements at the seafloor is one factor controlling the movement of these elements between the surface and subsurface. Over billions of years, these communities of slow growing microbes have altered the chemistry of the oceans and played a major role in Earth’s climate. 

But despite being numerous and widespread, there is still a surprising amount of organic matter in ocean sediments that these microbes never get around to eating. Deep Life Community members Steven D’Hondt and Robert Pockalny, along with colleagues Victoria Fulfer and Arthur Spivack (all at University of Rhode Island, USA), wondered, why don’t they eat all that organic matter buried beneath the seafloor? To explore this, and other unanswered questions regarding the biogeochemical impacts of subseafloor life, the authors published a new review paper [1] in Nature Communications. The review summarizes what is known about subseafloor microbial metabolic activities, explores how the limits to these activities affect Earth’s biogeochemical cycles, and discusses future research directions.

subseafloor microbial metabolism
Microbes beneath the seafloor have a major impact on the burial of organic matter, sulfate and nitrate, and the production of alkalinity and nitrogen into the water column. Credit: Josh Wood for publication by D’Hondt et al., 2019

According to D’Hondt, perhaps the subsurface microbes’ biggest impact on the surface world is that, by failing to eat some of the detritus and dead organic matter that falls to the seafloor, they cause Earth’s atmosphere and ocean to become more oxidized. This occurs because the production of organic compounds by plants through photosynthesis releases oxygen. The oxygen gets recycled when organisms break down those organic compounds in their cells through a process called respiration. But when organic matter gets buried and goes uneaten, the organic carbon has the potential to become trapped in the crust, and over longer time scales, recycled into the mantle. The oxygen that plants released during its formation, however, stays at the surface. 

“Subseafloor organisms eat buried organic matter so essentially they’re a throttle on that process,” said D’Hondt. “They control the rate at which the surface world gets oxidized.” Atmospheric oxygen levels have wobbled over geological timescales, but the general trend has been for Earth’s surface to become increasingly oxidized, and one factor is the burial of organic matter.

Microbes likely would be even more effective at driving biogeochemical cycles, through faster growth and more rapid metabolic rates, if they also were better at consuming subseafloor organic matter. 

Scientists have proposed several possible explanations for why microbes don’t eat all the organic compounds available to them. “Most people have said, some organic matter is just hard to eat and other organisms just don’t have the ability to eat it,” said D’Hondt. But microbes grow in the lab using these same hard-to-eat compounds. Researchers also have proposed that organic compounds stick to the surfaces of minerals, where microbes can’t access them, but D’Hondt and his co-authors don’t think that’s the whole story. 

“What we’re suggesting is kind of unorthodox,” said D’Hondt. “We’re saying that the apparent stability of organic matter for millions of years may be less a function of the composition of the organic matter than just how far is that environment removed from the surface world.”

The authors point to the fact that breaking down an organic compound will yield a different amount of energy depending on a microbe’s local conditions, which likely are related to its depth below the surface. For example, if concentrations of food are very low, or waste products have accumulated, then metabolizing the food source may not yield sufficient energy, and the cell might wait for better conditions. And if the cell is deep enough, it could wait a very long time for waste products to dissipate. 

“Life in marine sediment appears to persist at really slow metabolic rates and there’s this basic question, How do they survive for 100 million years?” said D’Hondt. He thinks that researchers may need to make more thorough tests of what limits rates of metabolic reactions in the subsurface and to see if there are other energy sources that are not yet accounted for, to understand how microbes last so long under such miserly conditions.

Additionally, D’Hondt emphasizes that we can direct these questions back in time to look at how subseafloor respiration has changed during Earth’s history and how those changes have altered the chemistry of the oceans and the oxidation of the surface world. Through future cooperative studies, biologists, Earth scientists and physical scientists, may be able to understand the constraints that dictate microbial meal selection in specific environments, and how the subsurface decision-making process has created the surface environment we know today.

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