There’s always food at home: the diet of an ocean trench microbe– anammox

Can anything survive at the bottom of the ocean? In total darkness, near-freezing temperatures, a cocktail of poisonous gases, and pressure reaching the equivalent of 50 jumbo jets stacked on a postage stamp, it is hard to imagine any form of life in such conditions. Where would an organism even obtain energy?

Yet life always finds a way. With over 7000 microbe species discovered in the hadal zone (approximately 6 to 11 km below sea level), biodiversity in this region is remarkable. Organisms at these depths have developed unique adaptations, including the ability to feast on ammonium. 

What are anammox?

Anammox (anaerobic ammonium oxidation) bacteria are well-adapted to deep-sea environments. They are in the Planctomycetota phylum and play a key role in the nitrogen cycle (Figure 1). They are found in a range of environments such as sea ice and marine sediments, including hadal sediments at depths reaching 10 km. In addition to withstanding the crushing pressures of ocean trenches, they can convert nitrite and ammonium ions directly into nitrogen and water via the anammox process. This process has been reported to produce 30-50% of the ocean’s diatomic nitrogen (N₂) – a limiting nutrient in marine environments. N₂ is used in nitrogen fixation by marine bacteria (like cyanobacteria), which convert it into usable nitrogen for plankton. Plankton are at the bottom of the marine food chain, so supporting their growth supports the growth of the entire food chain. 

The energy source

The ammonium ions come from mineralisation of organic matter (the process by which the nutrients in organic matter become available in inorganic forms) in marine sediments. The nitrate ions are produced as a result of aerobic nitrification (using oxygen to convert ammonia/ammonium ions to nitrate ions) in oxic zones (oxygen-rich marine zones).

Location of the process 

The anammox process takes place in the anammoxosome in the cytoplasm. This compartment contains anammox enzymes and has a lipid bilayer rich in ladderane lipids (Figure 2), which are currently found only in anammox. These lipids regulate membrane fluidity. For example, they decrease permeability to hydroxide and hydrogen ions (so the ions are less likely to get through the organelle’s membrane) to reduce pH variations. This can reduce the rate of chemical reactions by altering the shape of important enzymes. The lipids also prevent toxic by-products like hydrazine from damaging the rest of the cell. Hydrazine is an intermediate in this process and is also used in high-energy rocket fuel, so the bacteria definitely need to store it safely! 

Anammoxosome vs mitochondria

The anammoxosome is also adapted to increase efficiency. It is structurally and functionally very similar to mitochondria. Both are highly folded to increase surface area and reaction efficiency, and both act as the site of catabolic reactions (the breakdown of larger molecules into smaller molecules), ATP synthesis, and an electron transport chain. This is because a high surface area results in more frequent successful collisions of reactant particles, thus increasing the likelihood of reaction, according to collision theory. Therefore, anammox bacteria are still able to produce ATP without oxygen and with limited availability of other ‘food’ in ocean trenches.

Biochemistry of the anammox process

Generally, there are two possible reaction mechanisms for the anammox process. In both, a membrane-bound enzyme complex converts ammonium and hydroxylamine to hydrazine, and then hydrazine is oxidised to nitrogen gas in the periplasm. Nitrite is then reduced to hydroxylamine. However, it remains to be investigated whether this occurs at the same enzyme complex used for oxidising hydrazine or by using electrons from the oxidation of hydrazine, transferred via an electron transport chain to a nitrite-reducing enzyme in the cytoplasm (Figure 3). This process produces ATP in the cell because electrons released by the oxidation of hydrazine are transferred to the electron transport chain within the anammoosome membrane. This then creates a concentration gradient and a proton motive force as hydrogen ions (protons) are pumped across and build up on one side of the membrane. ATP is then synthesised as the hydrogen ions pass through the enzyme ATP synthase to add a phosphate to ADP to produce ATP, which is the energy currency of all organisms, including anammox.

NH₄⁺ + NO₂^--> N₂ +2H₂O

Other adaptations of anammox

Pressure and nutrient availability are not the only factors anammox need to account for. Being an ancient branch of microorganisms, with their last common ancestor living approximately 2.1 billion years ago, they have had a vast amount of time to develop into a variety of species, each adapted to their specific ecological niche. Iron nanoparticles and encapsulation proteins in the anammoxosome reduce iron toxicity and act as storage. The ability to change the size of the anammoxosome protects from high salinity. This reduces surface area and therefore the rate of reaction under the stress of high salinity so that the bacteria can conserve energy and only carry out essential reactions. Also, a smaller anammoxosome with a more fluid membrane prevents toxic hydrazine from leaking into the cytoplasm and protects the cell from osmotic stress (for example, by the loss of water in high salinity). Furthermore, altering ladderane composition reduces the impact of temperature changes. This is important because temperature must be controlled for the rate of chemical reactions to occur at their optimum. If it is too high, enzymes may change shape and denature; in this case, this would mean ATP cannot be synthesised. If it

is too low, the rate of reaction of the anammox process and other essential chemical reactions would be too slow to produce enough energy for the bacteria to survive, as reactant particles wouldn't have enough kinetic energy to collide successfully. 

Applications in biotechnology

Moreover, the ability of anammox to function under diverse conditions has been utilised in applications for wastewater treatment. Anammox are used to remove ammonium by converting ammonium into nitrogen gas while using nitrite as an electron acceptor. Advantages of this method include a lower carbon footprint compared to conventional processes, reduced need for aeration and therefore higher energy efficiency and lower operational costs. This is a wonderful example of how natural biological mechanisms can be studied and applied to our own real-world issues. 

Conclusion

In summary, anammox proves that life is able to find energy sources in the most (at first) seemingly barren environments. Anammox is just one example of this; other interesting microorganisms include sulphur-reducing microbes and iron-oxidising bacteria. They thrive in these environments and do not see the need to eat someplace else, because there’s always food at home. 

Written by Daniele Mazuolyte

Related article: The survival secrets of the Arctic springtail

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