Mechanisms of Acinetobacter baumannii Capsular Polysaccharide Cleavage by Phage Depolymerases

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Y. A. Knirel^1,a*, M. M. Shneider^2,3, A. V. Popova^3,4,5, A. A. Kasimova^1,6, S. N. Senchenkova¹, A. S. Shashkov¹, and A. O. Chizhov¹

¹Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, 119991 Moscow, Russia

²Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, 117997 Moscow, Russia

³Institute of Antimicrobial Chemotherapy, Smolensk State Medical University, 214019 Smolensk, Russia

⁴Moscow Institute of Physics and Technology (National Research University), 141701 Dolgoprudny, Moscow Region, Russia

⁵State Research Center for Applied Microbiology and Biotechnology, 142279 Obolensk, Moscow Region, Russia

⁶Higher Chemical College of the Russian Academy of Sciences, D. I. Mendeleev University of Chemical Technology of Russia, 125047 Moscow, Russia

^* To whom correspondence should be addressed.

Received March 11, 2020; Revised March 30, 2020; Accepted March 31, 2020

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Aerobic gram-negative bacterium Acinetobacter baumannii has recently become one of the most relevant pathogens associated with hospital-acquired infections worldwide. A. baumannii produces a capsule around the cell, which represents a thick viscous layer of structurally variable capsular polysaccharide (CPS). The capsule protects the bacteria against unfavorable environmental factors and biological systems, including bacteriophages and host immune system. Many A. baumannii phages have structural depolymerases (tailspikes) that specifically recognize and digest bacterial CPS. In this work, we studied the interaction of tailspike proteins of four lytic depolymerase-carrying phages with A. baumannii CPS. Depolymerases of three bacteriophages (Fri1, AS12, and BS46) were identified as specific glycosidases that cleave the CPS of A. baumannii strains 28, 1432, and B05, respectively, by the hydrolytic mechanism. The gp54 depolymerase from bacteriophage AP22 was characterized as a polysaccharide lyase that cleaves the CPS of A. baumannii strain 1053 by β-elimination at hexuronic acid (ManNAcA) residues.

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KEY WORDS: Acinetobacter baumannii, bacteriophage, tailspike, capsular polysaccharide, hexuronic acid, depolymerase, glycosidase, polysaccharide lyase, receptor binding protein, NMR spectroscopy

DOI: 10.1134/S0006297920050053

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