Genome Sequencing Identified a Novel Lasso Peptide

EurAsian Journal of BioSciences Eurasia J Biosci 14, 7933-7941 (2020)

Genome sequencing identified a novel lasso peptide

Sirilak Namwong1*, Masahiro Yuki2, Takuji. Kudo2, Moriya Ohkuma2 Takashi Itoh2 Somboon Tanasupawat3 1Department of Biotechnology, Faculty of Science and Technology, Suan Sunandha Rajabhat University, Bangkok 10300, Thailand. 2Japan Collection of Microorganisms, RIKEN BioResource Center, 3-1-1 Koyadai, Tsukuba, Ibaraki 305-0074, Japan 3Department of Biochemistry and Microbiology, Faculty of Pharmaceutical Sciences, Chulalongkorn University, Bangkok 10330, Thailand *Corresponding author: [email protected]

Abstract Background: One of the biggest problems to global health is rising of antibiotic resistance, however, the novel bioactive compounds are less discovered. To overcome this situation, genome sequencing and annotating have been developed in order to predict the biosynthesis pathway of new drugs. Materials and Methods: Strain BKK1 was classified based on 16S rRNA gene sequencing, ANI- Blast (ANIb), ANI-MUMmer (ANIm) and digital DNA-DNA hybridization (dDDH). The antiSMASH was selected for prediction the secondary metabolism gene clusters. Results: Strain BKK1 was proposed as Actinopolyspora saharensis based on 16S rRNA gene sequence similarity (99.07%), ANIb (98.59%,), ANIm (99.04%) and dDDH (90.9%). The gene clusters of biosynthetic pathways predicted to synthesize a class IV lasso peptide. Its leader region, core sequences and N-terminal end were divergent form class IV lasso peptides. According to the results, an active peptide from A. saharensis BKK1 was assumed to be a new biosynthesis cluster of class IV of lasso peptide. Additionally, its supernatant exhibited inhibitory activity against Escherichia coli ATCC 25922 and Staphylococcus aureus ATCC 25923. Conclusion: The genome sequence and antibacterial assessment of A. saharensis BKK1 provide the useful knowledge of the novel peptide antibiotic cluster for developing new medicines for further medical applications.

Keywords: Actinobacteria, Actinopolyspora saharensis, Lasso peptide, Genome, Bioactive compound

Namwong S, Yuki M, Kudo T, Ohkuma M, Itoh T, Tanasupawat S (2020) Genome sequencing identified a novel lasso peptide. Eurasia J Biosci 14: 7933-7941.

INTRODUCTION YIM90600. It carried erythromycin biosynthetic gene cluster encoding two novel erythromycins; erythronolide The discovery of novel active compounds from the H (EH) and erythronolide I (Chen et al. 2014). Recently, potential Actinobacteria i.e., Saccharopolyspora eight draft genome sequence of Actinopolyspora erythraea (erythromycins) and Streptomyces species were published, notwithstanding, there was no griseoflavus (aborycin) is screened by using the existing report of peptide antibiotics, a specific family of traditional methods. These procedures were costly and ribosomally synthesized and post-translationally time-comsuming (Fujimono and Sakai 2013, Chen et al. modified peptide (RiPP). The first lasso peptide named 2014). Despite the screening experiment, a few natural as anantin was proposed in 1986 and then microcin J25 products from the genus of Actinopolyspora were (MccJ25) in 1992 and aborycin in 1994 (De Lorenzo and investigated. The genus Actinopolyspora, which Neilands 1986, Salomon and Farias, 1992, Potterat et belonged to the class Actinobacteria, order al. 1994). Anantin and microcin belonged to class II Actinomycetales and family Actinopolysporaceae and lasso peptide and exhibited the atrial natriuretic factor twelve species have been described (Gochnauer et al. antagonist antimicrobial activity (Wyss et al. 1991, 1975, Yoshida et al. 1991, Guan et al. 2010, Tang et al. Maksimov and Link, 2014, Pati et al. 2018). Aborycin 2011, Meklat et al. 2012a, 2012b, Guan et al. 2013, (class I lasso peptide) consisted of a tricyclic 21-peptide Meklat et al. 2013a, 2013b, Saker et al. 2015, Duangmal antibiotic was proved as the HIV protease inhibitor to et al. 2016). prevent the assembly of HIV (Potterat et al. 1994, The genome analysis allowed us to discover a new Frechet et al. 1994, Shao et al. 2019). In 2017-2019, natural product form Actinopolyspora erythraea three novel antibacterial peptides (achromosin,

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EurAsian Journal of BioSciences 14: 7933-7941 (2020) Namwong et al. specialicin and citrocin) isolated from Actinobacteria W (Thompson et al. 1997). The phylogenetic tree was were published (Kaweewan et al. 2017, Kaweewan et al. constructed by the neighbor-joining algorithms using 2018, Cheung-Lee et al. 2019). Now, the active peptides MEGA 7.0 with bootstrap analysis (Saitou and Nei have been grained increasing attention for medical 1987). treatment due to their simply biosynthetic pathway Genome sequencing and functional gene annotation (Hegemann, 2019). Nevertheless, the novel biosynthetic Whole genome sequence of strain BKK1 was gene clusters (BGCs) of lasso peptide were rarely analyzed using an Illumina Miseq platform (Illumina, distributed (Tietz et al. 2017). Therefore, genome-mining Inc., San Diego, US-CA) using 2 × 250 bp paired-end approaches are considerably challenged for the reads. A de novo assembling of the reads to contigs discovery of new lasso peptides for the next years (Su using SPAdes 3.12 was performed (Bankevich et al. et al. 2019). 2012). The draft genomes of strain BKK1 was publicly This work aims to characterize Actinopolyspora available on the GenBank with the accession number of strain, BKK1 from salted egg collected from Bangkapi JAANYZ000000000. The genome was annotated on market in Bangkok province, Thailand based on the Prokka software 1.12 in line with the NCBI prokaryotic polyphasic approach, to analyze the draft genome genome annotation pipeline (PGAP) (Seemann 2014). sequence, to annotate the secondary metabolite genes Average nucleotide identity (ANI) was calculated and to determine the antibacterial activity. amongst the genome of two Actinopolyspora strains and the closely related type strains standing on ANI-Blast MATERIALS AND METHODS (ANIb) and ANI-MUMmer (ANIm) algorithms within the JSpeciesWS web service (Ritcher et al. 2016). The Polyphasic characteristics of strain BKK1 genome-to-genome distance calculator (GGDC 2.1) with Twenty-eight salted eggs were collected from the BLAST+ method was used to evaluate the digital Bangkapi market in Bangkok province, Thailand and DNA-DNA hybridization (dDDH) (Meier-Kolthoff et al. stored in the plastic bags at 4 C. Strain BKK1 was 2013). The polyphasic and genotypic (phylogenetic tree, isolated by spread-plate technique on complete medium ANI and dDDH) results were summarized for (CM, 15%, w/v NaCl) incubated at 30 C for 2 weeks identification of strain BKK1. (Meklat et al. 2012b). Phenotypic properties were The gene clusters were analyzed using antiSMASH assessed as described by Gordon et al. (1974), i.e., to permit us to predict the secondary metabolite utilization of carbon sources, range of NaCl for growth biosynthesis gene clusters (Medema et al. 2011). and resistance of antibiotics. All media used for biochemical tests included 15% (w/v) NaCl i.e., CM Antibacterial Activity assay agar, nutrient agar (NA) and the international Antimicrobial activity was determined by using paper Streptomyces project (ISP 2 and ISP 4). Cultural disc diffusion assay (Chen et al. 2010). Briefly, 100 μL characteristics and the colors of substrate. For culture of Staphylococcus aureus ATCC 25923 and Escherichia were investigated (Shirling and Gottlieb 1966). The coli ATCC 25922 we swabbed on the surface of NA. The colors of the substrate and aerial mycelia and any test extract was introduced into 7 mm discs incubated at soluble pigments were determined by comparison with 37 °C for 24 h. Inhibition zones were measured in the ISCC-NBS centroid color chart (Kelly and Judd millimeter (mm) using a vernier's caliper and tests were 1976). In chemotaxonomic studies, menaquinones and carried out in triplicate. polar lipids were analyzed (Minnikin et al. 1984, Komagata and Suzuki 1987). The isomeric form of RESULTS AND DISCUSSION diaminopimelic acid and the presence (or not) of glycine Polyphasic characteristics of strain BKK1 in the cell wall were realized as described by Becker et Strain BKK1 exhibited good growth on CM agar, NA al. (1964). The composition of whole-cell sugars was and ISP 2 media and developed long chains of spores determined according to the method of Lechevalier et al. on white aerial mycelium and fragmentation of yellow (1970). The fatty acid proﬁle was determined following substrate mycelium. It was sensitive to chloramphenicol the procedure of Sasser (1990), using the TSBA40 (30 µg/mL), but insensitive to lysozyme (0.005 % w/v). method on a Microbial Identiﬁcation System (MIDI). Strain BKK1 used sugars for their growth i.e., cellibiose, 16S rRNA gene sequencing and phylogenetic galactose, glucose, lactose, maltose and sucrose. It tree analysis grew in a wide range of NaCl concentrations (10-30%, 16S rRNA genes were amplified and purified. The w/v). This strain consisted of meso-diaminopimelic acid purified PCR products were sequenced using the (but not glycine) in its cell wall and arabinose including universal primers as researched by Coenye et al. galactose in whole-cell hydrolyzates. Three fatty acids (1999). The 16S rRNA sequence has been deposited in (anteiso-C17:0, iso-C15:0, and C15:0) and two the GenBank data library (strain BKK1=LC493220). The menaquinones [MK-10(H4) and MK-9(H4)] were 16S rRNA gene sequences of strain were aligned presented as the predominant fatty acids and the major against sequences of type strains using the CLUSTAL menaquinones, respectively. Typically, members of the

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Fig. 1. Phylogenetic tree of strain BKK1 and related bacteria species based on 16S rRNA gene sequences. The branching pattern was generated by the neighbor-joining method. Bar, 5 substitutions per 1000 nucleotide positions genus Actinopolyspora had a type IV cell wall (meso- clustered regularly interspaced short palindromic diaminopimelic acid without glycine), whole-cell sugar repeats (CRISPR). Average nucleotide identity values, pattern type A (arabinose and galactose), type PIII ANIb and ANIm, of the genomes among strain BKK1 and (phosphatidylcholine) phospholipid pattern and the all closest species were 78.32-98.59% and 85.37- absence of mycolic acids. The major fatty acid was 99.04%, respectively (Table 1). Strain BKK1 revealed anteiso-C17:0, iso-C15:0, and iso-C17:0. MK-9(H4) and MK- digital DNA- DNA hybridization (dDDH) values of 90.9% 10(H4) were the predominant menaquinones (C. I. model 88.6-92.7%) with Actinopolyspora (Gochnauer et al. 1975, Yoshida et al. 1991, Guan et al. saharensis DSM 45459T subsequent by A. halophila 2010, Tang et al. 2011, Meklat et al. 2012a, 2012b, ATCC 27976T (43.4%, C. I. model 40.9-46%) and A. Guan et al. 2013, Meklat et al. 2013a, 2013b, Saker et mortivallis JCM 7550T (24%, C. I model 21.7-26.5%). al. 2015, Duangmal et al. 2016). Hence, polyphasic The summarized of ANIb and ANIm values were listed characteristics indicated that strain BKK1 belonged in Table 1. It shared 90.9% dDDH and 98.59-99.04% within the genus Actinopolyspora. ANI with A. saharensis DSM 45459T that were higher 16S rRNA gene sequencing, phylogenetic tree than the generally accepted species boundary [dDDH analysis and genome sequencing (70%) and ANI (95-96 %,) values] (Lee et al. 2016, Phylogenetic tree analysis of complete 16S rRNA Meier-Kolthoff et al. 2013). Thus, it was identified as A. gene sequences of strain BKK1 (LC493220) and related saharensis. bacteria species shown in Fig. 1. It proved that strain Functional gene annotation BKK1 was associated to members of the genus The secondary metabolism gene clusters were Actinopolyspora. Strain BKK1 exhibited the highest 16S predicted by using antiSMASH. Through gene function rRNA gene sequence similarity value of 99.07% and analysis, a lasso peptide cluster were found. Its gene shared the same origin and evolutionary lineage with cluster revealed 21% with aborycin from Streptomyces Actinopolyspora saharensis DSM 45459T. sp. ZS0098. Aborycin was the class I lasso peptides The draft genome sequences of strain BKK1 had (Frechet et al. 1994) and its operon comprised a putative 4,838,785 bp in size with a G + C content of 69.4%. A precursor peptide gene (gene C1), a lasso peptide total of 4,430 predicted genes (85% of the whole biosynthesis B2 protein gene (gene A), a lasso genome) were identified with 4,363 predicted protein- isopeptide bond-forming gene (gene B1), ATP coding sequences (CDSs), 62 tRNAs, 1 rRNA and 4 transporter gene (gene U) and ACB transport gene (gene V) encoding an aborycin precursor, a protease

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Table 1. ANib, ANim and dDDH values among the draft genomes of strain BKK1 and their related type strains Reference %dDDH Prob. Genome of ANib% ANim% Model C.I genomes (formula2a) DDH>=70% 1 2 98.59 99.04 90.9 96.08 [88.6-92.7%] 1 3 91.15 92.0 43.4 6 [40.9-46%] 1 4 80.13 85.66 24 0.01 [21.7-26.5%] 1 5 78.95 85.54 23.6 0 [21.4-26.1%] 1 6 78.59 85.37 23.2 0 [20.9-25.7%] 1 7 78.32 85.46 23.3 0 [20.9-25.7%] 1 8 78.35 85.37 23.3 0 [21-25.8%] 1 9 78.34 85.41 23.3 0 [21-25.8%] Strains: 1, BKK1; 2, A. saharensis DSM 45459T; 3, A. halophila ATCC 27976T; 4, A. mortivallis JCM 7550T; 5, A. erythraea KCTC 19372T; 6, A. xinjiangensis KCTC 19656T; 7, A. alba DSM 45004T; 8, A. righensis DSM 45501T; 9, A. mzabensis DSM 45460T. All data were obtained from this study. aRecommended formula (identities/HSP length), which is liberated of genome length and is thus prosperous against the use of incomplete draft genomes

Table 2. The predicted genes of strain BKK1 associated with lasso peptide from Streptomyces sp. ZS0098 Lasso peptide genes form Legends Genes Streptomyces sp. ZS0098 Strain BKK1 A Lasso peptide biosynthesis B2 protein Lasso peptide biosynthesis B2 protein Biosynthetic genes B1 lasso peptide isopeptide bond-forming cyclase B2 - Asparagine synthase C2 - Predicted peptide (BKK1) D lasso peptide biosynthesis PqqD family chaperone Lasso peptide biosynthesis PqqD family chaperone Additional genes E - Dehydrogenase/reductase (2 genes) F - Dienelactone hydrolase G - Glycosyltransferase Aborycin family tricyclic lasso peptide (precursor C1 - peptide) H ABC transporter permease - I DoxX family membrane protein - J Thioredoxin domain-containing protein - K CapA family protein - L - Adenosylmethionine-dependent methyltransferase M - Oxidoreductase (2 genes) Other genes N - 5-dehydro-4-deoxy-D-glucuronate isomerase O - Furaric acid resistance protein family P - Pirin family protein Membrance protein (DUF2339 domain-containing Q - protein) R - L-lactate permease S - Low temperature requirement protein A T - Hypothetical protein U ATP-binding cassette domain-containing protein ATP-binding cassette domain-containing protein U ATP-binding cassette domain-containing protein - Transport genes ABC transporter V ABC transporter

W1 Response regulator transcription factor (2 genes) - Regulatory genes W2 IclR family transcriptional regulator X Sensor histidine kinase

(cleaving the peptide bond at leader-core junction), a macrolactam formation, the C-terminal region was lasso cyclase and transporters, respectively as shown in trapped by disulfide formation between two cysteines to Table 2 (Tietz et al. 2017). For the predicted gene preserve the compact structure (Hetrick and van der cluster of A. saharensis BKK1, gene C2 (a peptide Donk 2017) precursor), gene A, gene B2 (coding for asparagine Tietz et al. (2017) reported that all lasso peptide synthase/amide synthetase), gene U and gene V were shared a macrolactam ring/lasso isopeptide ring in the observed. In order to bear additional tailoring of lasso N-terminal region and four classes were proposed peptide, five essential biosynthetic genes were found according to the protoknot structure of disulfide bond at including bacterial coenzyme PQQ synthesis protein D the C-terminal tail (Fig. 3). Class I presented a lasso gene (PqqD, gene D), two dehydrogenase/reductase isopeptide ring and two disulfide linkages (Cys1→Cys13 genes (gene M) dienelactone hydrolase gene (gene F) and Cys7→Cys19) forming a tricyclic structure (Shao et and glycosyltransferase (gene G). These gene were al., 2019). Class II lasso peptide did not include disulfide well-matched function as the investigation of Shao et al. bond, while class III had a disulfide linkage (Jeanne Dit (2019). Fouque et al. 2019). Class IV was referred to as the rare Intiguingly, it was absence of cyclase gene (gene B1), lasso peptide topology having a disulfide handcuff nevertheless, homologous gene function (gene B2) was between Cys13→Cys16. Akin to that of other lasso represented at the same location (Fig. 2). Both enzymes peptides, a predicted precursor peptide from A. catalyzed the amide bond formation between amino saharensis BKK1 consisted of four conserved leader group of the N-terminal residue and the side chain of residues of class I-IV peptide antibiotics (Tyr, Pro, Gly Asp8/9 or Glu8 to form the lasso isopeptide ring. After and Thr) and an acidic amino acid (Asp) at position 9 of

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core biosynthetic genes additional biosynthetic genes transport-related genes regulatory genes other genes Fig. 2. Biosynthetic gene clusters of lasso peptide from Streptomyces sp. ZS0098 (a) and strain BKK1 (b)

Fig. 3. leader regions and core regions of class I-IV lasso peptide *Green letter; broadly conserved leader residues; Red letter, disulfide linkage *Underline, lasso isopeptide; Blue letter, disulfide handcuff

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EurAsian Journal of BioSciences 14: 7933-7941 (2020) Namwong et al. core peptide as listed in Fig. 3 (Nar et al. 2010). Within of Staphylococcus aureus ATCC 2592 and Escherichia a 21 amino acid-long core sequence, the macrolactam coli ATCC 25922 were ranged to 11.2-11.5±0.3 mm ring may form via the condensation of Asp9 side chain (DMSO, 8.2±0.2 mm) and 9.2-9.3±0.5 mm (DMSO, with the free amino group of Ile1 residue. Two cysteines within the C-terminal sequence (Cys16→Cys20) may 8.6±0.2 mm), respectively. The outcomes were agreed occur a disulfide handcuff formation as similar with with Dufour et al. (2012) and Shao et al. (2019) LP2006 (Tietz et al. 2017). Until now, Class I and II lasso presumed that lasso peptide gave advantage over peptide were contained over fourty structurally peptides competing against Staphylococcus aureus, and their N-terminal amino acid was Cys, Gly, Ser, Leu Enterococcus faecalis, Bacillus thuringiensis, E. coli, and Ala (Martin-Gómez et al. 2018). Finally, BI-32169 methicillin-resistant S. aureus (MRSA) and vancomycin and LP2006 were the sole member of the class III and resistant E. faecium (VRE). IV, respectively. As the results, a predicted peptide from A. CONCLUSION saharensis BKK1 belonged to the class IV lasso peptide. Strain BKK1 was classified as Actinopolyspora Its core peptide of 21 amino acids with Ile at the N- saharensis according to higher 90% of 16S rRNA gene terminal end and leader sequence (34 amino acids) sequence similarity, ANIb, ANIm and dDDH. A predicted were longer than LP2006 [17 amino acids with Gly at N- gene cluster of class IV lasso peptide was observed but terminus (core region) and 29 amino acids of leader its predicted amino acid sequence was dissimilar with a peptide] (Tietz et al. 2017). Additionally, it was sole member of class IV lasso peptide (LP2006). distinguished form LP2006 according to the sequential Therefore, A. saharensis BKK1, may create the novel position of its lasso peptide hallmark and leader region, and potent compounds for therapeutic of a variety of as well as its N-terminal amino acid. Therefore, it was diseases. predicted to bear a novel peptide cluster of class IV lasso Acknowledgements peptide. We would like to thank institute for research and Antibacterial Activity assay development, Suan Sunandha Rajabhat University for To confirm of genome function annotation results, financial support and providing laboratory equipment antibacterial activity was evaluated. The inhibition zone and experimental space.

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