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Thermoflexus hugenholtzii  JAD2 T , the only cultured representative of the  Chloroflexota  order  Thermoflexales , is abundant in Great Boiling Spring (GBS), NV, United States, and close relatives inhabit geothermal systems globally. However, no defined medium exists for  T. hugenholtzii  JAD2 T  and no single carbon source is known to support its growth, leaving key knowledge gaps in its metabolism and nutritional needs. Here, we report comparative genomic analysis of the draft genome of  T. hugenholtzii  JAD2 T  and eight closely related metagenome-assembled genomes (MAGs) from geothermal sites in China, Japan, and the United States, representing “ Candidatus  Thermoflexus japonica,” “ Candidatus  Thermoflexus tengchongensis,” and “ Candidatus  Thermoflexus sinensis.” Genomics was integrated with targeted exometabolomics and  13 C metabolic probing of  T. hugenholtzii . The  Thermoflexus  genomes each code for complete central carbon metabolic pathways and an unusually high abundance and diversity of peptidases, particularly Metallo- and Serine peptidase families, along with ABC transporters for peptides and some amino acids. The  T. hugenholtzii  JAD2 T  exometabolome provided evidence of extracellular proteolytic activity based on the accumulation of free amino acids. However, several neutral and polar amino acids appear not to be utilized, based on their accumulation in the medium and the lack of annotated transporters. Adenine and adenosine were scavenged, and thymine and nicotinic acid were released, suggesting interdependency with other organisms  in situ . Metabolic probing of  T. hugenholtzii  JAD2 T  using  13 C-labeled compounds provided evidence of oxidation of glucose, pyruvate, cysteine, and citrate, and functioning glycolytic, tricarboxylic acid (TCA), and oxidative pentose-phosphate pathways (PPPs). However, differential use of position-specific  13 C-labeled compounds showed that glycolysis and the TCA cycle were uncoupled. Thus, despite the high abundance of  Thermoflexus  in sediments of some geothermal systems, they appear to be highly focused on chemoorganotrophy, particularly protein degradation, and may interact extensively with other microorganisms  in situ .

frontiers in microbiology

Genomics, Exometabolomics, and Metabolic Probing Reveal Conserved Proteolytic Metabolism of Thermoflexus hugenholtzii and Three Candidate Species From China and Japan