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Missing Nitrogen May Be Vanishing in the Tubes of Giant Bacteria

The views expressed are those of the author and are not necessarily those of Scientific American.


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NOAA/Public Domain. Click image for source.

Off the coast of Mexico’s Baja Peninsula lies a dark, still, deep place. It is called the Soledad Basin, and in it lies a garden of bacteria so large you can see them with your own eyes.

A 250-m high ridge on the edge of the Soledad basin traps water inside. No strong currents disturb its depths. High above, coastal upwelling of cool, nutrient-rich water feeds a wealth of life, whose remains rain into the basin. There, they fuel life so well that virtually all oxygen is used up consuming it. For most animals, it is a dead zone. But for these giant bacteria and a few newly-discovered hangers-on, it is paradise.

That kind of bacteria is Thioploca, and for bacteria, they have an astounding lifestyle. While most bacteria top out at a few micrometers, they grow long, thick filaments 40-50 micrometers wide inside tubes that can reach half a millimeter in diameter and 20 centimeters (8 inches) long. They sprout prolifically from the floor of Soledad, reaching concentrations of about 50,000 sheaths per square meter.  In places where conditions are right, Thioploca has been found in growing in thick mats up and down the western coast of the Americas, as far south as Peru and Chile. There are more stunning images of Thioploca — including shots of much more luxuriantly carpeted sea floor cores than the image at the top of this post depicts — worth viewing over at Flickr.

What makes them particularly extraordinary is this: their food is hydrogen sulfide (H2S), found in the sediments of the seafloor. Their “oxygen” is nitrate (NO3), which is found, sparsely, in the seawater floating above. In order to both eat and breathe, the bacteria must shuttle between the ooze and the ocean. To do so, bundles of the bacteria secrete a slimy sheath in which they can commute between the two worlds by gliding up and down. This type of active bacterial movement is unique from that powered by propeller-like bacterial flagella. It doesn’t take a great leap of imagination to see the mind-boggling resemblance to many a marine worm, though instead of a single tubular body, it’s more like a bundle of spaghetti.

The filaments of Thioploca inside their slimy sheath. Creative Commons Carola Espinoza. Click image for source and license.

What nitrate does for Thioploca — and what oxygen does for us — is accept electrons harvested from food that have been passed down the electron transport chain to generate ATP, the molecule that powers cells. Without this final electron acceptor — something to “breathe” — respiration screeches to a halt, death by suffocation for both us and them. Yet there’s very little nitrate in the waters at the bottom of Soledad.

In spite of this, Thioploca manages to hoard nitrate by scrubbing it from seawater. Inside its cells are huge vacuoles, or storage bags — you could think of them as their equivalent of our oxygen tanks — stuffed with nitrate in concentrations up to 10,000 times that of the surrounding seawater. These storage bags are so large they take up 80% of the volume of Thioploca cells, making the cell appear hollow and squishing the remaining cytoplasm into a thin film around the cell membrane. This ensures that Thioploca can continue to breathe regardless of ambient conditions.

But Thioploca‘s nitrate heroics fit into a much larger story about nitrogen. Nitrogen compounds are limiting nutrients in most ecosystems on Earth. Nitrogen is a requirement for photosynthesis and is usually the one in shortest supply. Though we are bathed in nitrogen gas in the atmosphere, most organisms can’t use it. Only a very few bacteria can “fix” it, or break the strong triple bond of nitrogen gas (N2) to convert it to any number of other biologically usable nitrogen compounds, like ammonium, nitrate, or nitrite. How much “fixed” nitrogen is around determines how much algae and plants grow, and by extension how many herbivores and carnivores there are.

The reverse process — returning these compounds to nitrogen gas — is called denitrification. This “unfixing” of nitrogen, along with fixation, determines how much biologically available nitrogen is available for marine photosynthesis, and all the life it supports. Denitrification was thought to occur in open ocean but not in seafloor environments devoid of oxygen until 1999, when the discovery this was possible surprised scientists.

One would expect that denitrification would be limited by how fast nitrate can diffuse from surface waters where nitrogen fixing bacteria are active. But in the waters of Soledad, lots more N2 is appearing — and fixed nitrogen disappearing — than would be expected if only diffusion was in play. Something is getting busy with fixed nitrogen down there, and Thioploca‘s dragon-like nitrogen hoard seemed like a good place to start the search, even though Thioploca does not itself denitrify anything. Instead, it converts nitrate to nitrite (NO2-) or ammonium (NH4+) — still fixed nitrogen. Plants and algae living in nitrogen-poor areas often partner with the bacteria that can fix it; the most common example are legumes like beans that make special houses for nitrogen-fixing bacteria in their roots. A team of US and Danish scientists wondered: is there a similar such partnership enhancing denitrification in the deep sea by glomming on to Thioploca?

The team of US and Danish scientists wondered if a newly discovered class of organisms — the anammox bacteria — might be involved.  These bacteria harvest energy for life in the absence of oxygen by reacting ammonium with nitrite to make nitrogen gas and water: dentrification. Nitrite and ammonium are just what Thioploca makes. It seemed like a match, but no one had ever shown an association between the two bacteria before. So a team of US and Danish scientists set out to see if anammox bacteria were indeed there, and whether this could explain the disappearance of so much fixed nitrogen in the deep. They published their results in an August in Nature, and indeed, this seems to be the case.

They collected seafloor sediment samples from Soledad Basin, then stained the tubes of Thioploca with a DNA stain. Among the Thioploca, they found several types of round and filamentous bacteria, including one that glowed in a mysterious doughnut-shaped pattern. In anammox bacteria, there is a giant vacuole, or bag, called an annamoxosome where the denitrifying reactions — i.e., eating and breathing for the bacterium — transpire. It doesn’t stain because there’s very little DNA or nucleic acids inside, so the cell isn’t actually doughnut-shaped, but the pattern is characteristic of the group. This seemed like strong evidence anammox bacteria might be involved.

To gain more proof, the scientists used glowing probes known to stick to anammox bacteria in the genus Candidatus Scalindua. The doughnut-shaped pattern appeared once more. They also checked the DNA sequence of a few genes in these bacteria, and found again that the sequences indicated the bacteria were Candidatus Scalindua. Finally, they spiked ship-board Thioploca-containing sediments with labeled ammonium. And sure enough, nitrogen gas (N2) bearing the marked nitrogens appeared, indicating denitrification was occurring. Since no nitrate or nitrite was added, and one or the other is essential to anammox production of nitrogen gas, Scalindua must have gotten their supply from Thioploca. To gauge how much of the missing fixed nitrogen may be Scalindua‘s handiwork, they created and ran a complex model and judged the anammox bacterium responsible for 57+/- 21 % of bottom-water N2 production in Soledad — a substantial portion.

What kind of relationship do Thioploca and Scalindua have? Because nitrite can be toxic, this relationship could be a mutualism where both bacteria benefit from Scalindua‘s nitrite habit. On the other hand, the anammox bacteria may simply be sopping up nitrite seeping out of Thioploca with no effect on the titanic bacterium at all, which biologists would call commensalism. To me, if nitrite and ammonium are waste products for Thioploca, it’s hard to see how the presence of a bacterium that actively disposes of those wastes would fail to be a good thing.

The ability of giant Thioploca to squirrel away fixed nitrogen, and of anammox bacteria like Scalindua to get rid of it, is an adaptation that allows these bacteria to live in a place that little else on Earth can. It is an impressive feat and undoubtedly an important part of nature. At the same time, it makes life in the oceans less abundant than it otherwise might be by reducing the supply of fixed nitrogen. Thioploca species have been detected in oxygen-starved ocean sediments around the world. The authors of the Nature paper wonder whether a warming, and consequently less-oxygenated ocean may further encourage their growth — and make life harder for everything else.

Reference

Prokopenko M.G., Hirst M.B., De Brabandere L., Lawrence D.J.P., Berelson W.M., Granger J., Chang B.X., Dawson S., Crane III E.J. & Chong L. & (2013). Nitrogen losses in anoxic marine sediments driven by Thioploca–anammox bacterial consortia, Nature, 500 (7461) 194-198. DOI:

Jennifer Frazer About the Author: Jennifer Frazer is a AAAS Science Journalism Award-winning science writer. She has degrees in biology, plant pathology/mycology, and science writing, and has spent many happy hours studying life in situ. Follow on Twitter @JenniferFrazer.

The views expressed are those of the author and are not necessarily those of Scientific American.





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