Pentose degradation in archaea: Halorhabdus species degrade D-xylose, L-arabinose and D-ribose via bacterial-type pathwa

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ORIGINAL PAPER

Pentose degradation in archaea: Halorhabdus species degrade D‑xylose, L‑arabinose and D‑ribose via bacterial‑type pathways Jan‑Moritz Sutter1 · Ulrike Johnsen1 · Andreas Reinhardt1 · Peter Schönheit1 Received: 15 May 2020 / Accepted: 21 July 2020 © Springer Japan KK, part of Springer Nature 2020

Abstract The degradation of the pentoses d-xylose, l-arabinose and d-ribose in the domain of archaea, in Haloferax volcanii and in Haloarcula and Sulfolobus species, has been shown to proceed via oxidative pathways to generate α-ketoglutarate. Here, we report that the haloarchaeal Halorhabdus species utilize the bacterial-type non-oxidative degradation pathways for pentoses generating xylulose-5-phosphate. The genes of these pathways are each clustered and were constitutively expressed. Selected enzymes involved in d-xylose degradation, xylose isomerase and xylulokinase, and those involved in l-arabinose degradation, arabinose isomerase and ribulokinase, were characterized. Further, d-ribose degradation in Halorhabdus species involves ribokinase, ribose-5-phosphate isomerase and d-ribulose-5-phosphate-3-epimerase. Ribokinase of Halorhabdus tiamatea and ribose-5-phosphate isomerase of Halorhabdus utahensis were characterized. This is the first report of pentose degradation via the bacterial-type pathways in archaea, in Halorhabdus species that likely acquired these pathways from bacteria. The utilization of bacterial-type pathways of pentose degradation rather than the archaeal oxidative pathways generating α-ketoglutarate might be explained by an incomplete gluconeogenesis in Halorhabdus species preventing the utilization of α-ketoglutarate in the anabolism. Keywords  Halorhabdus utahensis · d-ribose · d-xylose and l-arabinose · Archaea · Xylose isomerase · Ribokinase · Lateral gene transfer

Introduction The pentoses d-xylose, l-arabinose and d-ribose are abundant in nature being part of hemicellulose material of plants and as component of ribonucleotides. Thus, these pentoses are common growth substrates of many microorganisms. The pathways of pentose degradation have been well studied in bacteria and fungi. In most bacteria d-xylose, l-arabinose and d-ribose are non-oxidatively degraded to xylulose-5-phosphate, an intermediate of the pentose phosphate Communicated by H. Atomi. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0079​2-020-01192​-y) contains supplementary material, which is available to authorized users. * Peter Schönheit [email protected]‑kiel.de 1



Institut für Allgemeine Mikrobiologie, Christian-AlbrechtsUniversität Kiel, Am Botanischen Garten 1‑9, 24118 Kiel, Germany

pathway, involving specific sugar kinases, isomerases and epimerases (Fig. 1a). The degradation of D-xylose involves xylose isomerase and xylulokinase, and of l-arabinose the enzymes arabinose isomerase, ribulokinase and l-ribulose5-phosphate-4-epimerase. Further, d-ribose conversion to xylulose-5-phosphate is catalyzed by ribokinase, ribose5-phosphate isomerase and