Critical roles of a housekeeping sortase of probiotic Bifidobacterium bifidum in bacterium–host cell crosstalk

Eiji Ishikawa,Tetsuya Yamada,Kazuaki Yamaji,Masaki Serata,Daichi Fujii,Yoshinori Umesaki,Hirokazu Tsuji,Koji Nomoto,Masahiro Ito,Nobuhiko Okada,Masato Nagaoka,Atsushi Gomi

doi:10.1016/j.isci.2021.103363

Eiji Ishikawa, Tetsuya Yamada + Show 10 more

Open Access

https://doi.org/10.1016/j.isci.2021.103363

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Abstract

SummaryBifidobacterium bifidum YIT 10347 (BF-1) is adhesive in vitro. Here we studied the molecular aspects of the BF-1 adhesion process. We identified and characterized non-adhesive mutants and found that a class E housekeeping sortase was critical for the adhesion to mucin. These mutants were significantly less adhesive to GCIY cells than was the wild type (WT), which protected GCIY cells against acid treatment more than did a non-adhesive mutant. The non-adhesive mutants aberrantly accumulated precursors of putative sortase-dependent proteins (SDPs). Recombinant SDPs bound to mucin. Disruption of the housekeeping sortase influenced expression of SDPs and pilus components. Mutants defective in a pilin or in an SDP showed the same adhesion properties as WT. Therefore, multiple SDPs and pili seem to work cooperatively to achieve adhesion, and the housekeeping sortase is responsible for cell wall anchoring of its substrates to ensure their proper biological function.

Highlights

Bifidobacteria, a major bacterial group in the human large intestine, may provide human health benefits, but their numbers decrease upon weaning and aging (Mitsuoka, 1992; Woodmansey, 2007)
We studied the molecular aspects of the bifidum YIT 10347 (BF-1) adhesion process
We identified and characterized non-adhesive mutants and found that a class E housekeeping sortase was critical for the adhesion to mucin

Summary

Introduction

Bifidobacteria, a major bacterial group in the human large intestine, may provide human health benefits, but their numbers decrease upon weaning and aging (Mitsuoka, 1992; Woodmansey, 2007). Several bifidobacteria have been utilized as probiotics (Fuller, 1989), and Bifidobacterium bifidum is one of the major species used. B. bifidum has the unique ability to relieve symptoms of gastric disorders in humans (Miki et al, 2007; Gomi et al, 2015, 2018; Urita et al, 2015). Several B. bifidum factors involved in adhesion to mucin or to cultured cells have been identified; these include sortase-dependent pili (Turroni et al, 2013), exo-a-sialidase (Nishiyama et al, 2017), BopA (Guglielmetti et al, 2008; Gleinser et al, 2012; Kainulainen et al, 2013), and transaldolase (Gonzalez-Rodriguez et al, 2012)

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