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Who prefers a sulfur diet?

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Evolution of sulfur metabolism in Archaea clarified by an international team including ITQB NOVA

The use of sulfur compounds to produce energy is believed to be one of the most ancient types of metabolisms used by primitive microorganisms to sustain life on the early anoxic earth. Yet, where and how this type of metabolism evolved is not clear.

Since the development of an oxygen atmosphere, the reduction of sulfate (SO42-, the most oxidized form of sulfur) is known to be the most important process in the global sulfur cycle and a dominant microbial metabolism in anaerobic environments, such as marine sediments. However, the geological evidence for dissimilatory sulfate reduction (DSR) by microbes dates at about 3.5 billion years ago, much earlier than the appearance of oxygen, although the nature of the organisms using this metabolism then is not known. “Life on earth started with primitive thermophilic anaerobic microrganisms, and their study is important to help us understand how they evolved into the ones that exist today” explains ITQB NOVA researcher Inês Cardoso Pereira, “This also allows us to better predict which type of life forms may exist in other planets where oxygen is not available”.

DSR is found in many classes of Bacteria, the largest kingdom of living organisms, but is more limited in Archaea, the second kingdom of microbial organisms. In contrast, phylogenetic studies suggest that the reduction of sulfite (SO32-) is more ancient in Archaea than in Bacteria, and was probably even present in LUCA, the Last Universal Common Ancestor.

In an article published today in Nature Microbiology, an international team of researchers, led by Nikolay Chernyh of the Winogradsky Institute of Microbiology in Moscow, Filipa Sousa of the University of Vienna (and ITQB NOVA alumni) and Inês Cardoso Pereira from ITQB NOVA, report on their investigation of sulfate reduction in acidic hyperthermal terrestrial springs of the Kamchatka Peninsula. The team used community profiling coupled with growth experiments, radioisotopes and proteomics to reveal that DSR in this environment is mainly due to a new archeon ‘Candidatus Vulcanisaeta moutnovskia’. They show that this organism has all the required genes for DSR, whereas previous reports of DSR in other cultivated Thermoproteaceae could not be confirmed. Detailed phylogenetic studies suggest that ‘Candidatus V. moutnovskia’ acquired key genes for DSR directly from Bacteria, and that this metabolism arose independently in Vulcanisaeta and Archaeoglobus, the only two genera of Archaea where it is confirmed. The key genes acquired are to the qmo genes coding for a membrane complex first discovered by the ITQB NOVA team, which enables the organisms to conserve energy from sulfate reduction. Overall, the study shows that DSR is rare in Archaea and suggest that the dissimilatory reduction of sulfite is more ancient than that of sulfate, which is in line with thermodynamics and the respective abundance of these compounds on the early earth.

The work involved researchers from the Russian Federal Research Center of Biotechnology and the Lomonosov Moscow State University, the University of Vienna, ITQB NOVA, Bangor University in the UK, the Centro Nacional de Biotecnología and the Institute of Catalysis of CSIC in Spain.

 

Original Paper

Nature Microbiology | https://doi.org/10.1038/s41564-020-0776-z

Dissimilatory sulfate reduction in the archaeon ‘Candidatus Vulcanisaeta moutnovskia’ sheds light on the evolution of sulfur metabolism

Nikolay A. Chernyh*, Sinje Neukirchen, Evgenii N. Frolov, Filipa L. Sousa*, Margarita L. Miroshnichenko, Alexander Y. Merkel, Nikolay V. Pimenov, Dimitry Y. Sorokin, Sergio Ciordia, María Carmen Mena, Manuel Ferrer, Peter N. Golyshin, Alexander V. Lebedinsky, Inês A. Cardoso Pereira* & Elizaveta A. Bonch-Osmolovskaya 

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