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<p>Many thermophiles that are abundant in high-temperature geothermal systems have never been cultivated and are poorly understood, including deeply branching members of the archaeal phylum <i>Thermoproteota</i>. Here, we describe the genome-guided cultivation of one such organism, <i>Calditenuis ramacidaminiphagus</i>, and show that it has evolved a heterotrophic metabolism focused on branched-chain amino acids (BCAAs). Initially, fluorescence in situ hybridization and nanoscale secondary ion mass spectrometry (FISH-nanoSIMS) showed that <i>Cal. ramacidaminiphagus</i> assimilated amino acids rapidly in casamino acid-amended enrichment cultures. Metagenome and metaproteome analyses showed a high abundance and expression of BCAA transporter genes, suggesting a BCAA-focused metabolism. This inference was supported by the subsequent enrichment of <i>Cal. ramacidaminiphagus</i> in BCAA-fed cultures, reaching 2.66×10<sup>6</sup> cells/mL and 48.7% of the community, whereas it was outcompeted when polar amino acids were included. Metabolic reconstruction and metaproteomics suggest that BCAAs are channeled into the mevalonate pathway for lipid biosynthesis and fuel ATP production through the TCA cycle coupled with aerobic respiration and through production of branched-chain organic acids by overflow metabolism. Ancestral state reconstructions and phylogenetic analyses of 62 <i>Caldarchaeales</i> genomes revealed multiple horizontal transfers of BCAA transporters to the ancestor of the genus <i>Calditenuis</i>. Our study highlights the crucial role of BCAAs in the early evolution and niche of this genus, and suggests a high degree of resource partitioning even within low-diversity thermophilic communities.</p>

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Branched-chain amino acid specialization drove diversification within Calditenuaceae (Caldarchaeia) and enables their cultivation

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年2月4日

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  • Dengxun Lai,
  • Damon Mosier,
  • Marike Palmer,
  • Xavier Mayali,
  • Juliet Johnston,
  • Walter Saldivar,
  • Jonathan K. Covington,
  • Jian-Yu Jiao,
  • Ranjani Murali,
  • Cale O. Seymour,
  • Lan Liu,
  • Zheng-Shuang Hua,
  • Wen-Jun Li,
  • Peter K. Weber,
  • Jennifer Pett-Ridge,
  • Daniel R. Colman,
  • Eric S. Boyd,
  • Takuro Nunoura,
  • Jeremy A. Dodsworth,
  • Brian P. Hedlund

摘要

Many thermophiles that are abundant in high-temperature geothermal systems have never been cultivated and are poorly understood, including deeply branching members of the archaeal phylum Thermoproteota. Here, we describe the genome-guided cultivation of one such organism, Calditenuis ramacidaminiphagus, and show that it has evolved a heterotrophic metabolism focused on branched-chain amino acids (BCAAs). Initially, fluorescence in situ hybridization and nanoscale secondary ion mass spectrometry (FISH-nanoSIMS) showed that Cal. ramacidaminiphagus assimilated amino acids rapidly in casamino acid-amended enrichment cultures. Metagenome and metaproteome analyses showed a high abundance and expression of BCAA transporter genes, suggesting a BCAA-focused metabolism. This inference was supported by the subsequent enrichment of Cal. ramacidaminiphagus in BCAA-fed cultures, reaching 2.66×106 cells/mL and 48.7% of the community, whereas it was outcompeted when polar amino acids were included. Metabolic reconstruction and metaproteomics suggest that BCAAs are channeled into the mevalonate pathway for lipid biosynthesis and fuel ATP production through the TCA cycle coupled with aerobic respiration and through production of branched-chain organic acids by overflow metabolism. Ancestral state reconstructions and phylogenetic analyses of 62 Caldarchaeales genomes revealed multiple horizontal transfers of BCAA transporters to the ancestor of the genus Calditenuis. Our study highlights the crucial role of BCAAs in the early evolution and niche of this genus, and suggests a high degree of resource partitioning even within low-diversity thermophilic communities.