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New metabolic pathway found in rumen microbiome

In ruminants, bacterium reacts to fluctuating sodium content with two different respiratory circuits.

Cows can adapt to a fluctuating sodium content in their feed, but how they do that has been a secret -- until now. Researchers from Goethe University in Germany have discovered a bacterium in the rumen microbiome that has a new type of cell respiration.

The cow can only process grass in its rumen with the help of billions of microorganisms. An entire zoo of bacteria, archaea and protozoa works there like on a production line. First, these single-cell organisms break down the cellulose, a polysaccharide. Other bacteria ferment the sugars released into fatty acids, alcohols and gases, such as hydrogen and carbon dioxide. Finally, methanogenic archaea transform these two gases into methane.

An average cow produces about 110 liters of methane per day, which escapes via rumination but also mixes again with partly digested food. As a result, the sodium content of the grass pulp can fluctuate to a considerable degree (between 60 and 800 millimoles of sodium chloride per liter), the Goethe University announcement said.

A research team from Germany and the U.S. has now discovered how the ruminal bacteria adapt to these extreme fluctuations in sodium content.

“Bioinformatic analyses of the genome of ruminal bacteria led our American colleague, Tim Hackmann, to assume that some ruminal bacteria have two different respiratory circuits. One of them functions with sodium ions, and the other without," explained professor Volker Müller with the Goethe University department of molecular microbiology and bioenergetics. That is why Müller suggested to his doctoral researcher Marie Schölmerich that she study a typical representative in the microbiome of ruminants: the bacterium Pseudobutyrivibrio ruminis.

Together with undergraduate student Judith Dönig and master's student Alexander Katsyv, Schölmerich cultivated the bacterium. They then were able to corroborate both respiratory circuits, Goethe University said.

As the researchers report in Proceedings of the National Academy of Sciences, the electron carrier ferredoxin is reduced during sugar oxidation. Reduced ferredoxin drives both respiratory circuits.

The one respiratory circuit comprises the enzyme complex Fd:NAD oxidoreductase (Rnf complex), which uses energy to transport sodium ions out of the cell. When they re-enter the cell, the sodium ions trigger an ATP synthase so that ATP is produced. This respiratory circuit works only in the presence of sodium ions.

In the absence of sodium ions, the bacterium forms an alternative respiratory circuit with another enzyme complex. The Ech hydrogenase (synonymous: Fd:H+ oxidoreductase) produces hydrogen and pumps protons out of the cell. If these ions re-enter the cell via a second ATP synthase that accepts protons but not sodium ions, ATP is also produced, the researchers said.

“This is the first bacterium so far in which these two simple, completely different respiratory circuits have been corroborated, but our bioinformatic analyses suggest that they are also found in other bacteria," Schölmerich explained. “It seems, therefore, that this adaptation strategy is more widespread."

Interestingly, both enzyme complexes (Rnf and Ech) were also discovered in bacteria that are old in terms of evolutionary biology. Müller's research group has examined them in depth but has always found only one of the two enzyme complexes and never both together.

“We're now going to use synthetic microbiology methods to produce hybrids of bacteria that contain both complexes in order to optimize them for biotechnological processes. In this way, we can raise the cellular ATP content, which will make it possible to produce products of a higher quality," Müller said.

The intention is to use the respiratory circuits to recover valuable substances through the fermentation of synthesis gas. This is the subject of the trials being conducted within the framework of a project sponsored by Germany's Federal Ministry of Education & Research.

Goethe University/ Cow: ShutterstockGoethe U pm_Pansenmikrobiom.jpg

The bacterium Pseudobutyrivibrio ruminis (green), a typical ruminal bacterium, obtains energy via two different respiratory circuits. The one requires sodium ions, the other hydrogen ions (H+). In this way, it can adapt to fluctuating sodium concentrations in animal feed in an optimum way.

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