How Microbes Survive When Buried Alive

A new model that probes the limits of microbial life finds that microorganisms in South Pacific Gyre sediments persist for millions of years in a dormant state, consuming the scraps of organic compounds buried with them.

For most microbes that settle into marine sediments, there’s nowhere to go but down. They become buried alive beneath new layers of ocean detritus, potentially laying low for tens of millions of years, with little access to food or energy sources. Estimates suggest that more microbes live in marine sediments than in all of the world’s soil, but researchers know little about how they survive in this dark, sinking habitat.

Now, a new model developed by DCO researchers predicts how microbes persist at the limits of life over geologic timescales. James Bradley, Jan Amend, and Douglas LaRowe (all at the University of California, Los Angeles, USA) applied the model to look at microbial survival and metabolism in sediments in the South Pacific Gyre, a veritable desert on the ocean floor that lies between Australia and South America. In a new paper in the journal Geobiology [1], they show that microorganisms survive in a state of suspended animation and subsist by slowly consuming nearby carbon compounds. Despite their low activity levels, these dormant microbes are responsible for breaking down more than 99 percent of the organic carbon in these ancient sediments. 

The researchers demonstrated their model using data from the South Pacific Gyre because low primary productivity from plankton in the surface ocean results in an extremely low input of organic carbon, and thus energy, to the seafloor, placing these sediments at the extreme end of habitability. “Sediments underlying the South Pacific Gyre have been isolated for up to 120 million years, and despite ultra-low concentrations of organic matter, they sustain thousands of microorganisms per square centimeter,” said Bradley, a postdoctoral fellow for DCO’s Deep Life Modeling and Visualization network. “Microorganisms inhabiting these sediments persist in some of the lowest energy states on Earth, making them an ideal site for testing the limits of microbial survival.” 
 
The new model uses a series of equations to describe mathematically when microbes switch from active to dormant states, how much energy they require at each state, and whether that energy comes from sources outside the cell, or from breaking down internal molecules. The open-source model can be downloaded freely and integrated into existing biogeochemical models as a new tool for determining the limits of life in any environment, over multi-million year timescales.

The model suggests that during the first million years of burial, microbes either go dormant and stop dividing, or die out. Only microbes that have adapted to harsh environments are likely to survive. After about 5 million years, the decline in cell numbers gets less sharp, and eventually stabilizes after tens of million of years. The results agree with previous measurements of cell numbers and organic carbon concentrations made from South Pacific Gyre sediments.

Even while dormant, microbes use the equivalent of about two percent of the total carbon in their cells each year to perform maintenance activities that keep them alive. They need to consume an outside energy source, namely the organic carbon buried with them, to persist for millions of years. Even though the activity of the microbes and the available carbon stores are extremely low, over millions of years, this activity adds up to represent an important piece of the carbon cycle. 

The findings suggest that scientists may be underestimating the role of dormant microbes in biogeochemical cycling. “We are used to thinking about active and growing organisms being responsible for carbon cycling,” said Bradley. “Here, we show that it is predominantly the least active organisms that survive over long timescales in ultra-low-energy marine sediments and drive the cycling of carbon within them.”

Finding the limits of microbial life may inform future studies of where and when life arose on a hostile early Earth, and where life might be located elsewhere in the solar system. If life does exist on Mars or Europa, it would most likely take refuge in the subsurface on these energy-limited planetary bodies. 

Now that the researchers have developed and tested their model for the limits of microbial life in marine sediments, they plan to scale up their efforts to create a global metabolic model of the subsurface biosphere. This model would assess the activity of microorganisms in their largest habitat on Earth.

sediment cores
Researchers study the limits of subseafloor life by collecting sediment cores, such as these, taken at the Dorado Outcrop in 2014 using the crewed deep-ocean research submersible Alvin. Credit: NSF OCE 1130146 and the National Deep Submergence Facility

 

Main image: Researchers modeled the limits to life for microbes buried in sediments beneath the South Pacific Gyre. They compared their results to measurements made by researchers aboard the International Ocean Discovery Program Expedition 329: South Pacific Gyre Subseafloor Life. Credit: John Beck, IODP/TAMU
 

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