Molecular analysis of cyclic α-maltosyl-(1→6)-maltose binding protein in the bacterial metabolic pathway

Masaki Kohno; Takatoshi Arakawa; Naoki Sunagawa; Tetsuya Mori; Kiyohiko Igarashi; Tomoyuki Nishimoto; Shinya Fushinobu

doi:10.1371/journal.pone.0241912

Molecular analysis of cyclic α-maltosyl-(1→6)-maltose binding protein in the bacterial metabolic pathway

Masaki Kohno, Takatoshi Arakawa, Naoki Sunagawa, Tetsuya Mori, Kiyohiko Igarashi, Tomoyuki Nishimoto, Shinya Fushinobu^*

^*Corresponding author for this work

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Abstract

Cyclic α-maltosyl-(1→6)-maltose (CMM) is a cyclic glucotetrasaccharide with alternating α-1,4 and α-1,6 linkages. Here, we report functional and structural analyses on CMM-binding protein (CMMBP), which is a substrate-binding protein (SBP) of an ABC importer system of the bacteria Arthrobacter globiformis. Isothermal titration calorimetry analysis revealed that CMMBP specifically bound to CMM with a Kd value of 9.6 nM. The crystal structure of CMMBP was determined at a resolution of 1.47 Å, and a panose molecule was bound in a cleft between two domains. To delineate its structural features, the crystal structure of CMMBP was compared with other SBPs specific for carbohydrates, such as cyclic α-nigerosyl-(1→6)-nigerose and cyclodextrins. These results indicate that A. globiformis has a unique metabolic pathway specialized for CMM.

Original language	English
Article number	e0241912
Pages (from-to)	e0241912
Journal	PLoS ONE
Volume	15
Issue number	11
DOIs	https://doi.org/10.1371/journal.pone.0241912
Publication status	Published - Nov 2020
MoE publication type	A1 Journal article-refereed

Funding

This study was partially supported by JSPS-KAKENHI (15H02443, 26660083, and 24380053 to S. F.; and 15H04526, 18H02252 and 19H03013 to K. I.), a Grant-in-Aid for Innovative Areas from the Japanese Ministry of Education, Culture, Sports, and Technology (MEXT) (No. 18H05494 to K.I.), and Platform Project for Supporting Drug Discovery and Life Science Research (Basis for Supporting Innovative Drug Discovery and Life Science Research (BINDS)) from the Japanese Ministry of Education, Culture, Sports, and Technology (MEXT). Hayashibara Co. Ltd. provided support in the form of salaries three authors (MK, TM,TN).

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title = "Molecular analysis of cyclic α-maltosyl-(1→6)-maltose binding protein in the bacterial metabolic pathway",

abstract = "Cyclic α-maltosyl-(1→6)-maltose (CMM) is a cyclic glucotetrasaccharide with alternating α-1,4 and α-1,6 linkages. Here, we report functional and structural analyses on CMM-binding protein (CMMBP), which is a substrate-binding protein (SBP) of an ABC importer system of the bacteria Arthrobacter globiformis. Isothermal titration calorimetry analysis revealed that CMMBP specifically bound to CMM with a Kd value of 9.6 nM. The crystal structure of CMMBP was determined at a resolution of 1.47 {\AA}, and a panose molecule was bound in a cleft between two domains. To delineate its structural features, the crystal structure of CMMBP was compared with other SBPs specific for carbohydrates, such as cyclic α-nigerosyl-(1→6)-nigerose and cyclodextrins. These results indicate that A. globiformis has a unique metabolic pathway specialized for CMM.",

author = "Masaki Kohno and Takatoshi Arakawa and Naoki Sunagawa and Tetsuya Mori and Kiyohiko Igarashi and Tomoyuki Nishimoto and Shinya Fushinobu",

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AU - Kohno, Masaki

AU - Arakawa, Takatoshi

AU - Sunagawa, Naoki

AU - Mori, Tetsuya

AU - Igarashi, Kiyohiko

AU - Nishimoto, Tomoyuki

AU - Fushinobu, Shinya

N1 - Publisher Copyright: © 2020 Kohno et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2020/11

Y1 - 2020/11

N2 - Cyclic α-maltosyl-(1→6)-maltose (CMM) is a cyclic glucotetrasaccharide with alternating α-1,4 and α-1,6 linkages. Here, we report functional and structural analyses on CMM-binding protein (CMMBP), which is a substrate-binding protein (SBP) of an ABC importer system of the bacteria Arthrobacter globiformis. Isothermal titration calorimetry analysis revealed that CMMBP specifically bound to CMM with a Kd value of 9.6 nM. The crystal structure of CMMBP was determined at a resolution of 1.47 Å, and a panose molecule was bound in a cleft between two domains. To delineate its structural features, the crystal structure of CMMBP was compared with other SBPs specific for carbohydrates, such as cyclic α-nigerosyl-(1→6)-nigerose and cyclodextrins. These results indicate that A. globiformis has a unique metabolic pathway specialized for CMM.

AB - Cyclic α-maltosyl-(1→6)-maltose (CMM) is a cyclic glucotetrasaccharide with alternating α-1,4 and α-1,6 linkages. Here, we report functional and structural analyses on CMM-binding protein (CMMBP), which is a substrate-binding protein (SBP) of an ABC importer system of the bacteria Arthrobacter globiformis. Isothermal titration calorimetry analysis revealed that CMMBP specifically bound to CMM with a Kd value of 9.6 nM. The crystal structure of CMMBP was determined at a resolution of 1.47 Å, and a panose molecule was bound in a cleft between two domains. To delineate its structural features, the crystal structure of CMMBP was compared with other SBPs specific for carbohydrates, such as cyclic α-nigerosyl-(1→6)-nigerose and cyclodextrins. These results indicate that A. globiformis has a unique metabolic pathway specialized for CMM.

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Molecular analysis of cyclic α-maltosyl-(1→6)-maltose binding protein in the bacterial metabolic pathway

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