Microbes That Live in 0% to 30% Salinity, Tube Worms Without Mouths, and Titan's Lakes of Oil: Takeshi Naganuma on Life in Extreme Environments

Naganuma describes a microbe called Halomonas variabilis as "possibly the toughest living thing on Earth." Halomonas titanicae is known as a microbe that is gradually breaking down the hull of the Titanic, which sank in 1912. H. variabilis is one of its relatives.

Naganuma encountered this microbe at an undersea volcano in the middle of the Atlantic Ocean. Running down the center of the Atlantic is a giant rift that seems to tear Africa from South America and Europe from North America, and the seafloor is still spreading apart on either side. Undersea volcanoes line this boundary. Naganuma dove to one of them in the crewed research submersible Shinkai 6500 and succeeded in collecting 300°C hydrothermal fluid.

The original target was microbes that feed on sulfur, a volcanic gas component contained in the hydrothermal fluid. However, the sulfur needed for culturing had been forgotten. So Naganuma changed tack. At undersea volcanoes, extremely salty water and water close to fresh water sometimes emerge alternately. Reasoning that there must be microbes adapted to large swings in salinity, Naganuma added table salt from the ship to the culture medium. Microbes grew. When those microbes were then transferred to fresh water, they still multiplied. Genetic analysis showed they were Halomonas variabilis.

What sets this microbe apart is the breadth of salinity it can tolerate. Ordinary seawater has a salinity of about 3%, but Halomonas variabilis can reportedly live in environments ranging from close to 0% up to saturated brine of nearly 30%.

What truly surprised Naganuma came next. Halomonas variabilis has been found all over the world, but the strain genetically closest to the one Naganuma collected at the Atlantic undersea volcano had been collected in Antarctica. Naganuma thought, "This makes no sense," and actually went to Antarctica to look for it. Sure enough, it was there.

According to the program's commentary, undersea volcanoes and Antarctica share intense fluctuations in salinity. Antarctica has land and lakes that once took in seawater. When water is lost to drying, the salinity becomes extremely concentrated, and in summer, melting snow and ice bring in fresh water. Naganuma went on to search for places with fluctuating salinity all over the planet, and says Halomonas variabilis was everywhere. The microbe was presented as an example of how wide a range of environments life can adapt to.

Naganuma went on to list more organisms that withstand extreme environments.

The first is extreme heat: Methanopyrus kandleri strain 116, a methane-producing archaeon found around deep-sea hydrothermal vents in the Indian Ocean. A research team at the Japan Agency for Marine-Earth Science and Technology (JAMSTEC) cultured it under high pressure close to deep-sea conditions and confirmed that it can multiply even at 122°C. In the deep sea, the intense water pressure keeps water from boiling even above 100°C.

The second is extreme pressure, and surprisingly, Naganuma's example was ordinary E. coli. A research team conducted an experiment in which they applied pressure to E. coli while selecting for stronger individuals. The result was reportedly a strain that could withstand pressure equivalent to a depth of more than 100,000 m. Even the deepest place on Earth is only about 10,000 m deep, at around 1,000 atmospheres. A depth of 100,000 m corresponds to 10,000 atmospheres. Earth's biosphere doesn't extend that far, so why could such an ability be acquired? Naganuma described this as "makes no sense."

The third is an organism that lives in oil. The "petroleum fly," which inhabits natural oil pools in California in the United States, spends its larval stage in petroleum. The larvae swim near the surface, feeding on insects and other creatures that fall into the oil and become stuck. They do not use the petroleum itself as food. Microbes capable of withstanding a petroleum-like environment are thought to live inside their bodies. Naganuma said this organism is quite exceptional even among Earth's life forms, and that it could become an important model organism for thinking about extraterrestrial life. This story ties into the discussion of Titan later on.

Most of Earth's ecosystems depend on plants capturing sunlight to produce organic matter. In the deep sea, where light doesn't reach, photosynthesis is impossible. So deep-sea organisms rely mainly on "marine snow" sinking from the surface layers for food.

In 1977, however, researchers surveying an undersea volcano off the Galápagos Islands found strange organisms growing in great numbers where hydrothermal fluid was welling up. These were tube worms. With red organs poking out of white tubes, they look like plants, but they are unmistakably animals. What's more, as they grow, they lose both their mouths and their digestive tracts.

Tube worms take in hydrogen sulfide emitted from hydrothermal vents and pass it to symbiotic bacteria. The bacteria use that chemical energy to produce organic matter, which the tube worms live on. Naganuma explained that this closely resembles plant photosynthesis. The only difference is that the energy source is volcanic gas rather than light. No one had ever imagined an ecosystem that doesn't depend on sunlight but instead on volcanic gas rising from Earth's interior. Naganuma called it "a revolutionary discovery."

It was also tube worms that led Naganuma to pursue deep-sea biology. On learning of their existence in high school, Naganuma reportedly thought, "This is the creature I've been searching for." Naganuma has dissected them many times. You pull a long, thin, earthworm-like body out of the hard white tube. The red part at the tip is the gills, below that is muscle, and further down is tissue without much structure that turns mushy when you open it up. Looking closely at that tissue, you find microbes inside the cells. These are the microbes that produce organic matter using volcanic gas as their energy source.

Tube worms can sometimes reach 3 m in length. On their lifespan, Naganuma prefaced the answer with "we don't really know," then introduced one study. At a site where dead tube worms had been drifting right after an undersea volcanic eruption, researchers measured how much the tubes had grown one year later. Calculating from that growth rate, one dataset indicated it would take 200 years to reach a certain size. It is said that they can easily live past 200.

Naganuma has seen crabs snipping off and eating the gills of weakened tube worms. A healthy one, Naganuma says, would quickly retract. Since there probably aren't many animals that can get inside the body after death, Naganuma speculates that the rest is broken down through something like fermentation.

In the middle of the Atlantic, Naganuma witnessed another scene. Countless shrimp called Rimicaris were swarming over chimney-like structures where hydrothermal fluid was gushing out. In human terms, these shrimp's eyes have moved toward the back of the head and function like an infrared camera. The shrimp gather in search of microbes, but some carelessly plunge into the hot fluid, are boiled the instant they do, and fall dead. Below, the shrimp carcasses pile up, and crabs come to eat them. Naganuma recalled feeling that an ecosystem had formed amid a rather surreal scene.

Naganuma has dived into the deep sea 14 times. The first dive was in April 1989, shortly after turning 28. Naganuma joined what is now JAMSTEC on April 1, back when it was called the Japan Marine Science and Technology Center. In the middle of new-employee training, Naganuma was summoned with "Forget about that, just come," and ended up diving without really knowing what was going on. The vessel was the Shinkai 2000. Like today's Shinkai 6500, it carried a crew of three, and underwater survey time was about eight hours. There is no toilet on board.

As a particularly memorable site, Naganuma named one of the undersea volcanoes in the Izu–Ogasawara volcanic chain. Descending to the bottom of the central crater, Naganuma found hydrothermal fluid spouting here and there. Even more surprising was the strength of the currents. Seeing objects tumbling along as if in a typhoon shattered Naganuma's worldview that the deep sea is an unchanging, quiet world. It was a moment that suggested that in the deep sea, from time to time or from place to place, strange things might be happening even at this very moment.

There were dangerous experiences, too. A submersible can check what's ahead using sonar and viewports, but it can't see directly below. Neither the Shinkai 2000 nor the 6500 is suited to hovering in the water while working, so they settle on the bottom. If hydrothermal fluid is spouting right underneath, that's dangerous. In fact, there was a time when, after the submersible had been hauled up onto the mother ship, the underside of the hull was found to be scorched. Since then, an additional protective layer was fitted outside the viewports, and temperature sensors were installed at the front, middle, and rear of the hull.

Even so, Naganuma still thinks of the deep sea as a quiet world. In a conversation with astronaut Mohri, who has been to both space and the deep sea, Mohri said the darkness of space and the darkness of the deep sea are different. The blackness of space gives a sense of truly nothing, of "void," while the blackness of the deep sea gives a sense that it is full of something.

The conversation then moved beyond Earth. Naganuma named three key elements for life to emerge: a steady supply of energy, the materials to build living things, and liquid water. The hydrothermal vents, or undersea volcanoes, in the deep sea of the early Earth met all three conditions. In our solar system, there are bodies where the same conditions may be present.

Naganuma's "top picks" are Europa at Jupiter and Enceladus at Saturn. Enceladus has been studied in detail. Water from the ocean beneath its ice has been observed spouting from cracks in the surface ice, and a spacecraft flew through those plumes and analyzed them on the spot. The composition was 99% water, but the remaining 1% contained carbon monoxide, carbon dioxide, and methane. According to Naganuma, it's hard to imagine carbon dioxide and methane coexisting. If they do coexist, there must be some kind of reaction system, which suggests something related to life. Organic matter has also been found. Organic matter is either the material that makes up life or fragments of it. For these reasons, Naganuma thinks the chances for Enceladus are quite high.

Europa also has potential, but it hasn't been studied as thoroughly yet. The Europa Clipper spacecraft was launched in October 2024 and is en route, aiming to arrive in 2030.

Naganuma also draws attention to how small Enceladus is. It is only about 500 km across, roughly the distance from Tokyo to Osaka. And yet, for some reason, it has heat from volcanic activity inside. The reason is still not well understood, but there are various theories. Applying those theories to other bodies leads to one argument after another that this or that body could also have a heat source.

As an example, Naganuma cited the asteroid (dwarf planet) Ceres. It is said that Ceres may have an internal heat source, that some of its ice may have melted into liquid water, and that there may be small-scale hydrothermal activity. As one piece of evidence, carbonate minerals, which cannot form without liquid water, have been found in considerable amounts on Ceres's surface.

On the surface of Pluto, at the edge of the solar system, there is a large heart-shaped feature. Pluto as a whole is bumpy, yet only the heart-shaped area is flat. This is said to be because some heat source melted the surface ice, which flattened out and then froze again. Naganuma believes that as long as there is heat, the possibilities can be discussed endlessly.

What Naganuma calls "insanely interesting" is Saturn's moon Titan. The most interesting thing about it is that its surface has many lakes of liquid. Titan's surface is close to or below minus 200°C, and liquid water doesn't exist there. The lakes are made of liquid methane and ethane, the simplest oils. In our world they're gases, but at low temperatures they become liquid.

According to Naganuma, humanity knows a great deal about the biology of water ("water biology") but understands little about biology in oil ("oil biology"). So there is a discussion about using organisms that live in oil, like Earth's petroleum fly, as a starting point for thinking about what oil biology might be possible on Titan.

The problem is polarity. In a water molecule, the oxygen side is slightly negative and the hydrogen side slightly positive. This lets water dissolve many substances, making it an excellent environment for the chemical reactions life requires. Liquid methane and ethane, on the other hand, have almost no polarity, so the emergence of life there is thought to be difficult.

Naganuma points out, however, that there is a molecule that can remain liquid even at Titan's low temperatures and that also has polarity. It is phosphine, a phosphorus compound, which has also been found in the atmospheres of Jupiter and Saturn. If there were phosphine in the oil lakes, a watery world could form there, and something close to the biology we know might be possible.

Naganuma went further, into the structure of cells. Our cells exist in a "water-in-water" state, watery both outside and inside, so a cell membrane made of oil separates the inside from the outside. In Titan's case, it would be "water-in-oil," so there would be no need for an oily partition. If reactions proceeded inside droplets of phosphine in the oil, that alone might become something like a cell. In that case, Naganuma thinks, cells could have a simpler structure than those of Earth's organisms. The program added that this is, at this stage, a "what if" scenario.

Asked whether they would like to go to space, Naganuma answered that they would like to go if they could. Naganuma once took the astronaut selection exam and was eliminated in the semifinal round. Naganuma has given up on going as an astronaut but has high hopes for the space tourism likely to emerge in the future.

Naganuma is especially interested in Mars. Just as with the deep sea or Antarctica, Naganuma points out, sending people is easy; bringing them back alive is the hard part. What's more, it's important to bring them back in the same condition as before they went, and that is difficult. Naganuma believes this will be the bottleneck for human expansion to Mars. On the other hand, there is also talk that a one-way trip might be fine, and that those who go could simply stay and live on Mars. Naganuma thinks that, given their age, they might be approached, and said they would go if asked.

On where life began, Naganuma thinks places like undersea volcanoes are a good fit. Naganuma's position is that this is where the life we know today originated. According to the program's commentary, around 4 billion years ago, when life is thought to have emerged, Earth was repeatedly struck by large meteorites, and any life that arose on the surface may have been wiped out each time. Deeper beneath the seafloor would be less affected by these impacts, and Naganuma thinks that may be where the origin of present-day life lay.

As another way of thinking, Naganuma introduced the panspermia hypothesis: the idea that life itself, or the materials for life, were carried to Earth from elsewhere along with meteorites and the like. What Naganuma finds interesting is that it also includes the idea that only the raw materials were delivered and then assembled on Earth.

In this connection, Naganuma cited a recent finding. Analysis of samples brought back by the Hayabusa2 spacecraft from the asteroid Ryugu reportedly found all types of nucleobases. Nucleobases are molecules that act like the letters used to write information into DNA and RNA, and there are five: adenine, guanine, cytosine, thymine, and uracil. The United States also carried out a sample return from the asteroid Bennu, and all five types, A, G, C, T, and U, were found there as well. Bennu is a small body only about 500 m across, and such bodies have presumably come to Earth in the past. From this, Naganuma thinks the theory that at least the raw materials were delivered from space is plausible.

On extraterrestrial life, Naganuma states clearly that it is "possible." Naganuma believes the origin of life is fairly universal in the cosmos and expects that even if life emerged beyond Earth, it would use DNA or RNA to carry its genetic information. That is exactly why Naganuma regards the discovery of RNA building blocks in asteroids as "amazing."

Within the solar system, the promising candidates are Mars and Europa. Europa Clipper will arrive in 2030 and begin observations in 2031. Naganuma sees this as probably the earliest opportunity. As for Mars, it depends on future plans, but Naganuma hopes a discovery of life might come earlier, or around the same time. That said, Naganuma personally believes there is no life on the surface of Mars. Even so, Naganuma added that if the surface were searched thoroughly, life might be found in some little sheltered nook.

On civilizations, Naganuma said that other factors come into play, so "we don't really know," but as someone in the camp that wants there to be civilizations, Naganuma looks for them on exoplanets. Several Earth-like planets have already been found, and on them, environmental changes similar to Earth's, and an evolutionary history similar to that of Earth's life, could play out. On the other hand, Naganuma points out that the evolution of life on Earth includes several events that can only be seen as chance. Land organisms arose, four-legged animals came onto land, some of them climbed trees, and then came down from the trees and became humans. Naganuma considers this not inevitable but largely the result of chance, and says the very emergence of Homo sapiens seems like a miracle. For that reason, civilization may not be universal, and Earth may be the only one in this universe. Even if there are others, Naganuma has a feeling there might be only one or two.

Finally, Naganuma answered the question "What is life?" from the perspective of physics. What Naganuma considers the most powerful law in the universe is the principle of increasing entropy. A drop of ink spreads out, but never returns to its original state. Life, however, takes shape, that shape forms the shape of the next generation, and it keeps multiplying. This appears to run counter to entropy.

According to Naganuma, there is a theory that entropy can decrease locally as long as it increases overall, and life probably falls into that category. Seen that way, Naganuma says, perhaps the presence of life actually makes the entropy of the universe as a whole increase faster. Perhaps the universe, wanting to reach a state of nothingness sooner, is using life locally to tinker with entropy. To the universe, life may be something like a "fruitless flower," one that blooms but bears no fruit. Naganuma said they can't help feeling that might be the case.

Even so, Naganuma says it's fine if life is a fruitless flower. Naganuma finds beauty in the very fact that life locally defies entropy, takes shape, passes itself on, and multiplies. And Naganuma added that, given how discoveries beyond our imagination keep emerging one after another, what they said today might also be overturned. Naganuma said there are probably not many extraterrestrial civilizations, but evidence might emerge that there are countless. Observation of Europa begins in 2031, but a radio message from space might arrive even sooner. It might be tomorrow. So rather than thinking of things as settled, it's fine to keep in mind that there are still many possibilities. With those words, Naganuma brought the talk to a close.