When the going gets dense: microbial life under extreme pressure

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From project deadlines to taxes to balancing work and family life, pressure is something we’re all familiar with. Many of us feel like we’re constantly living under pressure. But not like microbes. Microbes take the notion of “living under pressure” to another level entirely.

Life in the deep, dark ocean is mysterious and beautiful. It's also adapted to survive at pressures hundreds to thousands of times greater than humans can tolerate. Credit: National Geographic

Life in the deep, dark ocean is mysterious and beautiful. It’s also adapted to survive at pressures hundreds to thousands of times greater than humans can tolerate. Credit: National Geographic

As I’ve discussed in previous posts, energy limitation and sometimes temperature are two of the main factors restricting microbial life. However, in the deep ocean, the most unique environmental challenge microbes face may be the sheer weight of water bearing down on them.

Welcome to the piezosphere, defined as the part of the ocean where pressure exceeds 10 megapascals (MPa), a hundred times greater than air pressure at sea level. While the piezosphere may seem remote, it is by no means insignificant. It encompasses roughly 75% of the ocean’s total volume, making it the largest habitat for microbial life on earth.

Graphical representation of the piezosphere, where temperature, light and food are scarce, and pressure is high. Credit: Picard and Daniel 2013

Graphical representation of the piezosphere, where temperature, light and food are scarce, and pressure is high. Credit: Picard and Daniel 2013

 Some like it hot, some like it cold

The inhabitants of the piezosphere, aptly named piezophiles, are sub-classified according to the pressure range they tolerate.  The most extreme hyperpiezophiles can tolerate pressures up to 130 MPa, or 1,300 x atmospheric! In the deep ocean, temperatures range from near freezing (2-3 ºC) to piping hot (> 400 ºC near hydrothermal vents). Piezophiles occupy almost the entire spectra of temperatures known to support life (with the exception of some very cold loving bacteria buried in ice and permafrost). Accordingly, scientists further classify piezophiles based on their temperature preference.

All known cold-loving “psychro-piezophiles” are Bacteria, most from the phyla Gammaproteobacteria. These guys thrive in the the deepest, darkest, coldest parts of the ocean and include the most pressure-tolerant organisms on Earth. Species of Shewanella and Moritella, isolated from Challenger Deep, the ocean’s deepest location in the Marianas trench, thrive at pressures of 110 MPa and temperatures of 2 ºC. Other cold-seep bacteria include members of the genus Carnobacterium.  Recently discovered in the Aleutian Trench, these bacteria are close relatives of pyschrophiles found abundantly in Alaskan permafrost.

The deepest part of the ocean floor may not look like much, but it's home to some of the strangest bacteria known to biology. Credit: National Geographic

The deepest part of the ocean floor may not look like much, but it’s home to some of the strangest bacteria known to science. Credit: National Geographic

On the other end of the spectrum, some piezophiles like it hot. Heat and pressure loving microbes, or hyperthermo-hyperpiezophiles  (try saying that five times fast) are more diverse than their cold-weather counterparts, distributed across both Bacteria and Archaea. The hyper-hypers are found near deep sea hydrothermal vents, where fissures in the crust spew hot magma onto the ocean floor. This group includes Methanopyrus kandleri, the most thermophilic (heat loving) bacteria every described, capable of growing at 40 MPa and a whopping 122ºC.

Specialized membranes

How do piezophiles survive under pressures that would be deadly for most life? To answer that question, it’s important to first  understand why high pressure is deadly for most of us. It has to do with our cell membranes. For membranes to function properly, they must remain fluid. Too solid, and many biological processes are interrupted, including cell respiration, nutrient transport and signaling. Low temperatures and high pressures both cause membranes to solidify by “packing”  their building blocks rigidly together.

There is growing evidence that pressure lovers have highly specialized cell membranes. Remember, membranes are composed of fatty acids, molecules with a hydrophilic (water-loving) head and a hydrophobic tail. Fatty acid “tails” are really of a chain of carbon atoms that can vary in length and bonding structure. Many cell membrane properties can be deduced by examining the length and structure of these fatty acid tails.

Several recent studies find piezophile membranes contain unusually high levels of unsaturated fatty acids, or UFAs. UFAs distinguish themselves from saturated fatty acids by their carbon-carbon double bonds, which cause their tails to take on a  kinked structure rather than standing straight. Ultimately, these kinks prevent UFAs from packing too closely together. Hence, more UFAs = more fluid membrane. Piezophile UFAs are unusually long, an adaptation also thought to help maintain their fluidity.

Piezophile membranes are different from regular membranes in that they maintain their structure at extremely high pressures. Credit: Abe 2013

Piezophile membranes are different from regular membranes in that they maintain their structure at extremely high pressures. Credit: Abe 2013

Life Strategies

Pressure aside, life in the piezosphere is not for the faint of heart. Often too cold, sometimes too hot, never enough food. Organic matter enters the deep ocean mainly as intermittent “rain” from the euphotic zone (the sunlit ocean) above. Microbes living off this organic rain are very efficient scavengers, but nonetheless are incredibly slow-growing, suggesting they live in a state of perpetual starvation.

Many organisms in the piezosphere have abandoned carbon entirely, instead eating inorganic compounds like hydrogen sulfide. Some adventurous archaea even make their own food, turning carbon dioxide into sugar just like plants do, but using mineral energy instead of light.

How does pressure affect the diverse metabolism of the piezosphere? The jury’s still out on this one. Generally, in the presence of oxygen, high pressure seems to stimulate deep ocean microbial activity. In the absence of oxygen, the effects of pressure can vary. Iron-reducers (organisms that “breathe iron” instead of oxygen) appear to grow faster at higher pressures, but for other anaerobic (non-oxygen breathing) bacteria, such as sulfate reducers, high pressure appears detrimental.

The high pressure frontier

There are many open questions for scientists interested in the limits of life under extreme pressure. The deep ocean is vast and difficult to sample; its’ microbial diversity is largely unknown. Most sampling efforts have focused on cold seeps and hydrothermal vents. Only a handful of studies examine piezophiles living at more moderate temperatures. Moreover, metagenomic tools, now widely used to examine the diversity of microbial communities, are biased towards abundant individuals. It’s possible that our current genetic tools only capture a fraction of the diversity present in the piezosphere, masking rare but potentially ecologically important players.

Studying the ecology of piezophiles in their “natural environment”  is also a challenge. Specialized equipment can be used to reproduce the high pressures of the piezosphere, but these tools do not necessarily mimic other aspects of the native environment, such as nutrient availability. Most often, researchers are forced to decompress their samples and grow piezophiles under a normal atmosphere. Whether the activity of piezophiles under artificially low pressure is comparable to life in the deep ocean remains to be seen.

All in all,  life in the piezosphere is still shrouded in mystery. Many scientists believe life originated in high pressure environments such as hydrothermal vents or deep ocean trenches. Understanding life in the piezosphere today might help scientists to determine how life on Earth got its start – and, in turn, how life may evolve on other worlds.

ResearchBlogging.org

Picard A, & Daniel I (2013). Pressure as an environmental parameter for microbial life–a review. Biophysical chemistry, 183, 30-41 PMID: 23891571

Fang, J., Zhang, L., & Bazylinski, D. (2010). Deep-sea piezosphere and piezophiles: geomicrobiology and biogeochemistry Trends in Microbiology, 18 (9), 413-422 DOI: 10.1016/j.tim.2010.06.006

Abe, F. (2013). Dynamic structural changes in microbial membranes in response to high hydrostatic pressure analyzed using time-resolved fluorescence anisotropy measurement Biophysical Chemistry, 183, 3-8 DOI: 10.1016/j.bpc.2013.05.005

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