Sulfolobus acidocaldarius Transports Pentoses via a Carbohydrate Uptake Transporter 2 (CUT2)-Type ABC Transporter and Metabolizes Them through the Aldolase-Independent Weimberg Pathway
Authors: Wagner Michaela , Shen Lu , Albersmeier Andreas , van der Kolk Nienke , Kim Sujin , Cha Jaeho , Bräsen Christopher , Kalinowski Jörn , Siebers Bettina , Albers Sonja-Verena 
Published: November 2017

ABSTRACT

Sulfolobus
spp. possess a great metabolic versatility and grow heterotrophically on various carbon sources, such as different sugars and peptides. Known sugar transporters in
Archaea
predominantly belong to ABC transport systems. Although several ABC transporters for sugar uptake have been characterized in the crenarchaeon
Sulfolobus solfataricus
, only one homologue of these transporters, the maltose/maltooligomer transporter, could be identified in the closely related
Sulfolobus acidocaldarius
. Comparison of the transcriptome of
S. acidocaldarius
MW001 grown on peptides alone and peptides in the presence of
d
-xylose allowed for the identification of the ABC transporter for
d
-xylose and
l
-arabinose transport and the gaining of deeper insights into pentose catabolism under the respective growth conditions. The
d
-xylose/
l
-arabinose substrate binding protein (SBP) (Saci_2122) of the ABC transporter is unique in
Archaea
and shares more similarity to bacterial SBPs of the carbohydrate uptake transporter-2 (CUT2) family than to any characterized archaeal one. The identified pentose transporter is the first CUT2 family ABC transporter analyzed in the domain of
Archaea
. Single-gene deletion mutants of the ABC transporter subunits exemplified the importance of the transport system for
d
-xylose and
l
-arabinose uptake. Next to the transporter operon, enzymes of the aldolase-independent pentose catabolism branch were found to be upregulated in N-Z-Amine and
d
-xylose medium. The α-ketoglutarate semialdehyde dehydrogenase (KGSADH; Saci_1938) seemed not to be essential for growth on pentoses. However, the deletion mutant of the 2-keto-3-deoxyarabinoate/xylonate dehydratase (KDXD [also known as KDAD]; Saci_1939) was no longer able to catabolize
d
-xylose or
l
-arabinose, suggesting the absence of the aldolase-dependent branch in
S. acidocaldarius
.

IMPORTANCE
Thermoacidophilic microorganisms are emerging model organisms for biotechnological applications, as their optimal growth conditions resemble conditions used in certain biotechnologies such as industrial plant waste degradation. Because of its high genome stability,
Sulfolobus acidocaldarius
is especially suited as a platform organism for such applications. For use in (ligno)cellulose degradation, it was important to understand pentose uptake and metabolism in
S. acidocaldarius
. This study revealed that only the aldolase-independent Weimberg pathway is required for growth of
S. acidocaldarius
MW001 on
d
-xylose and
l
-arabinose. Moreover,
S. acidocaldarius
employs a CUT2 ABC transporter for pentose uptake, which is more similar to bacterial than to archaeal ABC transporters. The identification of pentose-inducible promoters will expedite the metabolic engineering of
S. acidocaldarius
for its development into a platform organism for (ligno)cellulose degradation.