Abstract
Metagenomic analyses have advanced our understanding of ecological microbial diversity, but to what extent can metagenomic data be used to predict the metabolic capacity of difficult-to-study organisms and their abiotic environmental interactions? We tackle this question, using a comparative genomic approach, by considering the molecular basis of aerobiosis within archaea. Lipoylation, the covalent attachment of lipoic acid to 2-oxoacid dehydrogenase multienzyme complexes (OADHCs), is essential for metabolism in aerobic bacteria and eukarya. Lipoylation is catalysed either by lipoate protein ligase (LplA), which in archaea is typically encoded by two genes (LplA-N and LplA-C), or by a lipoyl(octanoyl) transferase (LipB or LipM) plus a lipoic acid synthetase (LipA). Does the genomic presence of lipoylation and OADHC genes across archaea from diverse habitats correlate with aerobiosis? First, analyses of 11,826 biotin protein ligase (BPL)-LplA-LipB transferase family members and 147 archaeal genomes identified 85 species with lipoylation capabilities and provided support for multiple ancestral acquisitions of lipoylation pathways during archaeal evolution. Second, with the exception of the Sulfolobales order, the majority of species possessing lipoylation systems exclusively retain LplA, or either LipB or LipM, consistent with archaeal genome streamlining. Third, obligate anaerobic archaea display widespread loss of lipoylation and OADHC genes. Conversely, a high level of correspondence is observed between aerobiosis and the presence of LplA/LipB/LipM, LipA and OADHC E2, consistent with the role of lipoylation in aerobic metabolism. This correspondence between OADHC lipoylation capacity and aerobiosis indicates that genomic pathway profiling in archaea is informative and that well characterized pathways may be predictive in relation to abiotic conditions in difficult-to-study extremophiles. Given the highly variable retention of gene repertoires across the archaea, the extension of comparative genomic pathway profiling to broader metabolic and homeostasis networks should be useful in revealing characteristics from metagenomic datasets related to adaptations to diverse environments.
Highlights
Culture-independent, metagenomic analyses have been successful in advancing our knowledge of microbial abundance across diverse ecological niches
In eukaryotes and most bacteria, lipoate protein ligase (LplA) is encoded by a single gene, whereas studies in the archaeon Thermoplasma acidophilum revealed distinct genes, LplA-N and LplA-C, encoding proteins that correspond to the N- and C-terminal domains of E. coli LplA and that are both required for E2 lipoylation [23,24,25]
Despite the closer phylogenetic relationship of Clade II to LipM, we propose that proteins in this clade are LplA-N, and not octanoyl transferases, based on the correlated presence of LplA-C and the absence of lipoic acid synthetase (LipA) in the genomes of these taxa (Table S1); this classification should be considered provisional in the absence of additional biochemical data
Summary
Culture-independent, metagenomic analyses have been successful in advancing our knowledge of microbial abundance across diverse ecological niches (reviewed by [1]). The second, the reductive phase, is characterized by genome streamlining and the retention of a more minimal, and potentially heterogeneous, gene repertoire (1400–1800 gene families) [10] This persistent genomic streamlining has radically altered the repertoires of even the most highly conserved gene classes, including those involved in translation, replication, cell division and DNA repair, and is central to functional diversity across the domain [11]. We propose that gene repertoire heterogeneity, associated with metabolism and homeostasis, may reflect archaeal adaptation to, and exploitation of, a remarkable diversity of environments. We assess this possibility by considering aerobiosis within archaea because (i) archaea display tremendous diversity in their utilization and tolerance of aerobic environments and (ii) aerobiosis pathways have been well characterized biochemically. The distribution and genomic characteristics of lipoylation systems have yet to be studied across archaea
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