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Review
. 2019 Feb 26:10:302.
doi: 10.3389/fmicb.2019.00302. eCollection 2019.

Overview of the Antimicrobial Compounds Produced by Members of the Bacillus subtilis Group

Simon Caulier  1   2 , Catherine Nannan  1 , Annika Gillis  1 , Florent Licciardi  1 , Claude Bragard  2 , Jacques Mahillon  1
Affiliations
Review

Overview of the Antimicrobial Compounds Produced by Members of the Bacillus subtilis Group

Simon Caulier et al. Front Microbiol. .

Abstract

Over the last seven decades, applications using members of the Bacillus subtilis group have emerged in both food processes and crop protection industries. Their ability to form survival endospores and the plethora of antimicrobial compounds they produce has generated an increased industrial interest as food preservatives, therapeutic agents and biopesticides. In the growing context of food biopreservation and biological crop protection, this review suggests a comprehensive way to visualize the antimicrobial spectrum described within the B. subtilis group, including volatile compounds. This classification distinguishes the bioactive metabolites based on their biosynthetic pathways and chemical nature: i.e., ribosomal peptides (RPs), volatile compounds, polyketides (PKs), non-ribosomal peptides (NRPs), and hybrids between PKs and NRPs. For each clade, the chemical structure, biosynthesis and antimicrobial activity are described and exemplified. This review aims at constituting a convenient and updated classification of antimicrobial metabolites from the B. subtilis group, whose complex phylogeny is prone to further development.

Keywords: Bacillus subtilis group; bacteriocins; biocontrol; biosynthetic pathways; lipopeptides; polyketides; siderophores; volatile.

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Figures

Figure 1
Figure 1
Timeline emergence of the species from the B. subtilis group. The species are classified following their relatedness to the closest original member of the group (gray boxes). Heterotypic synonyms are not shown.
Figure 2
Figure 2
Antimicrobial molecules classes from the B. subtilis group. The subdivision between the classes is based on the biosynthetic pathway (i.e., ribosomal peptides, polyketides, hybrids, non-ribosomal peptides, and volatile compounds).
Figure 3
Figure 3
Lanthionine biosynthesis. General pathway of the lanthionine synthesis (A), structure of subtilin (B) and nisin A (C). Non-modified AA are indicated in teal whereas dehydrated serine (Dha, dehydroalanine) and threonine (Dhb, dehydrobutyrine) are colored in orange. The lanthionine (Ala-S-Ala, alanine-S-alanine) and R-methyllanthionine (Abu-S-Ala, aminobutyrate-S-alanine) bridges are shown in purple. The AA of nisin that differ from those in subtilin are highlighted as hatched circles. Adapted from Cotter et al. (2005) and Spieß et al. (2015).
Figure 4
Figure 4
AHLs structure and its corresponding enzymatic degradations by QQ. The broken lines show the cleavages sites of four enzymes: (1) lactonase; (2) decarboxylase; (3) acylase; (4) deaminase. Adapted from Czajkowski and Jafra (2009).
Figure 5
Figure 5
Chemical structures of some B. subtilis group polyketides. Variants from macrolactin and difficidin are presented.
Figure 6
Figure 6
Schematic representation of the modules and domains mediating PKS and NRP biosynthesis. (A) The domains involved in the PK synthesis are the acyltransferase (AT), the acyl carrier protein (ACP), the ketosynthase (KS) and the chain-terminating thiosterase (TE) domains. In gray, the auxiliary domains can mediate ketoreduction (KR), dehydration (DH), and enoylacyl reduction (ER) at each elongation step (n). (B) The core domains for NRP biosynthesis are the adenylation (A), the peptidyl carrier domain (PCP), the condensation (C), and the final thioesterase (TE) domains. The auxiliary domains consist in cyclization (Cy), N-methylation (MT), and epimerization (E) domains.
Figure 7
Figure 7
Polyketides and lipopeptides biosynthesis mechanism. (A) The AT domain catalyzes the binding of the monomer substrate and the ACP domain. The KS domain is acetylated on the acyl residue of a polyketide starter or in elongation and catalyzes the transfer of the substrate subunit carried by the ACP. (B) The A domain activates an AA chain extension subunit and its transfer to the PCP carrier domain. The C domain catalyzes the bond mediating the chain elongation. Adapted from Cane and Walsh (1999) and Challis and Naismith (2004).
Figure 8
Figure 8
Chemical structures of some B. subtilis group NRPs. (A) Lipopeptides. (B) Miscellaneous NRPs.
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