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In Silico Screening Unveil the Great Potential of Ruminal Bacteria Synthesizing Lasso Peptides

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In Silico Screening Unveil the Great Potential of Ruminal Bacteria Synthesizing Lasso Peptides In silico Screening Unveil the Great Potential of Ruminal Bacteria Synthesizing Lasso Peptides Sabino, Y. N. V., Araújo, K. C. D., Assis, F. G. D. V. D., Moreira, S. M., Lopes, T. D. S., Mendes, T. A. D. O., Huws, S. A., & Mantovani, H. C. (2020). In silico Screening Unveil the Great Potential of Ruminal Bacteria Synthesizing Lasso Peptides. Frontiers in Microbiology, 11, [576738]. https://doi.org/10.3389/fmicb.2020.576738 Published in: Frontiers in Microbiology Document Version: Publisher's PDF, also known as Version of record Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal Publisher rights Copyright 2020 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:23. Sep. 2021 fmicb-11-576738 September 10, 2020 Time: 15:4 # 1 ORIGINAL RESEARCH published: 11 September 2020 doi: 10.3389/fmicb.2020.576738 In silico Screening Unveil the Great Potential of Ruminal Bacteria Synthesizing Lasso Peptides Yasmin Neves Vieira Sabino1, Katialaine Corrêa de Araújo1, Fábia Giovana do Val de Assis1, Sofia Magalhães Moreira1, Thaynara da Silva Lopes1, Tiago Antônio de Oliveira Mendes2, Sharon Ann Huws3 and Hilário C. Mantovani1* 1 Departamento de Microbiologia, Universidade Federal de Viçosa, Viçosa, Brazil, 2 Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, Brazil, 3 Institute for Global Food Security, School of Biological Sciences, Medical Biology Centre, Queen’s University Belfast, Belfast, United Kingdom Studies of rumen microbial ecology suggest that the capacity to produce antimicrobial peptides could be a useful trait in species competing for ecological niches in the ruminal ecosystem. However, little is known about the synthesis of lasso peptides Edited by: by ruminal microorganisms. Here we analyzed the distribution and diversity of lasso Harsh Mathur, peptide gene clusters in 425 bacterial genomes from the rumen ecosystem. Genome Teagasc, Ireland mining was performed using antiSMASH 5, BAGEL4, and a database of well-known Reviewed by: precursor sequences. The genomic context of the biosynthetic clusters was investigated Piyush Baindara, University of Missouri, United States to identify putative lasA genes and protein sequences from enzymes of the biosynthetic Takeshi Zendo, machinery were evaluated to identify conserved motifs. Metatranscriptome analysis Kyushu University, Japan Nicholas Heng, evaluated the expression of the biosynthetic genes in the rumen microbiome. Several University of Otago, New Zealand incomplete (n = 23) and complete (n = 11) putative lasso peptide clusters were detected *Correspondence: in the genomes of ruminal bacteria. The complete gene clusters were exclusively Hilário C. Mantovani found within the phylum Firmicutes, mainly (48%) in strains of the genus Butyrivibrio. [email protected] The analysis of the genetic organization of complete putative lasso peptide clusters Specialty section: revealed the presence of co-occurring genes, including kinases (85%), transcriptional This article was submitted to regulators (49%), and glycosyltransferases (36%). Moreover, a conserved pattern of Antimicrobials, Resistance and Chemotherapy, cluster organization was detected between strains of the same genus/species. The a section of the journal maturation enzymes LasB, LasC, and LasD showed regions highly conserved, including Frontiers in Microbiology the presence of a transglutaminase core in LasB, an asparagine synthetase domain in Received: 26 June 2020 Accepted: 17 August 2020 LasC, and an ABC-type transporter system in LasD. Phylogenetic trees of the essential Published: 11 September 2020 biosynthetic proteins revealed that sequences split into monophyletic groups according Citation: to their shared single common ancestor. Metatranscriptome analyses indicated the Sabino YNV, Araújo KC, expression of the lasso peptides biosynthetic genes within the active rumen microbiota. Assis FGV, Moreira SM, Lopes TS, Mendes TAO, Huws SA and Overall, our in silico screening allowed the discovery of novel biosynthetic gene clusters Mantovani HC (2020) In silico in the genomes of ruminal bacteria and revealed several strains with the genetic potential Screening Unveil the Great Potential of Ruminal Bacteria Synthesizing to synthesize lasso peptides, suggesting that the ruminal microbiota represents a Lasso Peptides. potential source of these promising peptides. Front. Microbiol. 11:576738. doi: 10.3389/fmicb.2020.576738 Keywords: precursor sequence, RiPPs, rumen, Butyrivibrio, antiSMASH 5, BAGEL4 Frontiers in Microbiology| www.frontiersin.org 1 September 2020| Volume 11| Article 576738 fmicb-11-576738 September 10, 2020 Time: 15:4 # 2 Sabino et al. Lasso Peptides in Ruminal Bacteria INTRODUCTION carboxyl group of the Glu/Asp residue at position 8 or 9, while LasB catalyzes the transfer of ammonia from glutamine to the Natural products have improved human quality of life and activated side-chain carboxyl group. Following this, the cleavage play a noteworthy role in drug discovery and development of the precursor peptide releases an N-terminal Gly/Cys, and the (Newman and Cragg, 2016). Among natural products, secondary cyclization takes place by a nucleophilic attack (Larsen et al., metabolites stand out as scaffolds for the development of 1999; Makarova et al., 1999; Duquesne et al., 2007a; Yan et al., products for human medicine, animal health, crop protection, 2012). The gene D is also frequently found on the biosynthetic and numerous biotechnological applications (Bachmann et al., gene clusters of lasso peptides encoding an ABC transporter that 2014). Traditional culture-based strategies for the screening of is thought to play a role in immunity of producer cells against the new molecules have been responsible for the discovery of many antimicrobial activity of their lasso peptides (Solbiati et al., 1996, relevant enzymes and metabolites (Steele and Stowers, 1991; 1999; Bountra et al., 2017). Winter et al., 2011). However, these approaches are largely Studies based on genome mining have contributed to driven by chance, making then costly, time-consuming, and identifying new microbial species producing lasso peptides often limited regarding the number of strains that can be (Knappe et al., 2008; Maksimov et al., 2012b; Tietz et al., 2017). used in large-scale screening endeavors (Tietz et al., 2017). The The ruminal ecosystem is composed of microbial communities advent of microbial genomics and the increasing availability of that show high taxonomic and functional diversity (Morais computational tools to perform genome mining has evidenced and Mizrahi, 2019), and although it has been investigated as the underexplored potential of some microbial species as a source for novel enzymes and antimicrobials (Oyama et al., alternative sources of new therapeutic agents (Winter et al., 2017; Neumann and Suen, 2018; Palevich et al., 2019), the 2011). These tools and resources emerged as an alternative rumen still represents an underexplored environment for the approach to identify novel biosynthetic gene clusters (BGCs) discovery of lasso peptides. Indeed, both culture-dependent encoding putative bioactive metabolites and to assess the genetic and culture-independent approaches have revealed promising potential of producer strains (Weber and Kim, 2016). Besides the antimicrobial peptides from the rumen (Mantovani et al., 2002; discovery of new products, genome mining also contributes to Russell and Mantovani, 2002; Azevedo et al., 2015; Oyama et al., understanding the connection between metabolites and the gene 2017, 2019). However, no systematic efforts have been made sequences that encode them, providing ecological insights about to investigate the potential of rumen bacteria to produce lasso the role of individual microbial populations in the microbiome peptides. The availability of hundreds of reference genomes from (Bachmann et al., 2014). cultured ruminal bacteria through the Hungate1000 Project1, Secondary metabolites could play a diverse role in the offers an unprecedented opportunity to identify novel lasso environment by their wide range of biological activities. In peptides within the genomes of ruminal bacteria. The present this context, lasso peptides stand out as functionally diverse study set out to perform an in silico screening of the genomes metabolites produced by several species of bacteria. Members of the major bacterial species represented in the core ruminal of the lasso peptide family are reported to have antimicrobial microbiome in an attempt to identify biosynthetic gene clusters (Salomon
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