Culture and genome-based analysis of four soil Clostridium isolates reveal their potential for antimicrobial production
Abstract Background Soil bacteria are a major source of specialized metabolites including antimicrobial compounds. Yet, one of the most diverse genera of bacteria ubiquitously present in soil, Clostridium, has been largely overlooked in bioactive compound discovery. As Clostridium spp. thrive in ext...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2021-09-01
|
Series: | BMC Genomics |
Subjects: | |
Online Access: | https://doi.org/10.1186/s12864-021-08005-2 |
_version_ | 1819122608252125184 |
---|---|
author | Amila S. N. W. Pahalagedara Ruy Jauregui Paul Maclean Eric Altermann Steve Flint Jon Palmer Gale Brightwell Tanushree Barua Gupta |
author_facet | Amila S. N. W. Pahalagedara Ruy Jauregui Paul Maclean Eric Altermann Steve Flint Jon Palmer Gale Brightwell Tanushree Barua Gupta |
author_sort | Amila S. N. W. Pahalagedara |
collection | DOAJ |
description | Abstract Background Soil bacteria are a major source of specialized metabolites including antimicrobial compounds. Yet, one of the most diverse genera of bacteria ubiquitously present in soil, Clostridium, has been largely overlooked in bioactive compound discovery. As Clostridium spp. thrive in extreme environments with their metabolic mechanisms adapted to the harsh conditions, they are likely to synthesize molecules with unknown structures, properties, and functions. Therefore, their potential to synthesize small molecules with biological activities should be of great interest in the search for novel antimicrobial compounds. The current study focused on investigating the antimicrobial potential of four soil Clostridium isolates, FS01, FS2.2 FS03, and FS04, using a genome-led approach, validated by culture-based methods. Results Conditioned/spent media from all four Clostridium isolates showed varying levels of antimicrobial activity against indicator microorganism; all four isolates significantly inhibited the growth of Pseudomonas aeruginosa. FS01, FS2.2, and FS04 were active against Bacillus mycoides and FS03 reduced the growth of Bacillus cereus. Phylogenetic analysis together with DNA-DNA hybridization (dDDH), average nucleotide identity (ANI), and functional genome distribution (FGD) analyses confirmed that FS01, FS2.2, and FS04 belong to the species Paraclostridium bifermentans, Clostridium cadaveris, and Clostridium senegalense respectively, while FS03 may represent a novel species of the genus Clostridium. Bioinformatics analysis using antiSMASH 5.0 predicted the presence of eight biosynthetic gene clusters (BGCs) encoding for the synthesis of ribosomally synthesized post-translationally modified peptides (RiPPs) and non-ribosomal peptides (NRPs) in four genomes. All predicted BGCs showed no similarity with any known BGCs suggesting novelty of the molecules from those predicted gene clusters. In addition, the analysis of genomes for putative virulence factors revealed the presence of four putative Clostridium toxin related genes in FS01 and FS2.2 genomes. No genes associated with the main Clostridium toxins were identified in the FS03 and FS04 genomes. Conclusions The presence of BGCs encoding for uncharacterized RiPPs and NRPSs in the genomes of antagonistic Clostridium spp. isolated from farm soil indicated their potential to produce novel secondary metabolites. This study serves as a basis for the identification and characterization of potent antimicrobials from these soil Clostridium spp. and expands the current knowledge base, encouraging future research into bioactive compound production in members of the genus Clostridium. |
first_indexed | 2024-12-22T06:55:09Z |
format | Article |
id | doaj.art-4a9d4f25edb647b9acbe0586f9664021 |
institution | Directory Open Access Journal |
issn | 1471-2164 |
language | English |
last_indexed | 2024-12-22T06:55:09Z |
publishDate | 2021-09-01 |
publisher | BMC |
record_format | Article |
series | BMC Genomics |
spelling | doaj.art-4a9d4f25edb647b9acbe0586f96640212022-12-21T18:35:00ZengBMCBMC Genomics1471-21642021-09-0122111410.1186/s12864-021-08005-2Culture and genome-based analysis of four soil Clostridium isolates reveal their potential for antimicrobial productionAmila S. N. W. Pahalagedara0Ruy Jauregui1Paul Maclean2Eric Altermann3Steve Flint4Jon Palmer5Gale Brightwell6Tanushree Barua Gupta7Food System Integrity team, Hopkirk Research Institute, AgResearch Ltd, Massey UniversityData Science team, Grasslands Research Centre, AgResearch LtdData Science team, Grasslands Research Centre, AgResearch LtdFood System Integrity team, Hopkirk Research Institute, AgResearch Ltd, Massey UniversitySchool of Food and Advanced Technology, Massey UniversitySchool of Food and Advanced Technology, Massey UniversityFood System Integrity team, Hopkirk Research Institute, AgResearch Ltd, Massey UniversityFood System Integrity team, Hopkirk Research Institute, AgResearch Ltd, Massey UniversityAbstract Background Soil bacteria are a major source of specialized metabolites including antimicrobial compounds. Yet, one of the most diverse genera of bacteria ubiquitously present in soil, Clostridium, has been largely overlooked in bioactive compound discovery. As Clostridium spp. thrive in extreme environments with their metabolic mechanisms adapted to the harsh conditions, they are likely to synthesize molecules with unknown structures, properties, and functions. Therefore, their potential to synthesize small molecules with biological activities should be of great interest in the search for novel antimicrobial compounds. The current study focused on investigating the antimicrobial potential of four soil Clostridium isolates, FS01, FS2.2 FS03, and FS04, using a genome-led approach, validated by culture-based methods. Results Conditioned/spent media from all four Clostridium isolates showed varying levels of antimicrobial activity against indicator microorganism; all four isolates significantly inhibited the growth of Pseudomonas aeruginosa. FS01, FS2.2, and FS04 were active against Bacillus mycoides and FS03 reduced the growth of Bacillus cereus. Phylogenetic analysis together with DNA-DNA hybridization (dDDH), average nucleotide identity (ANI), and functional genome distribution (FGD) analyses confirmed that FS01, FS2.2, and FS04 belong to the species Paraclostridium bifermentans, Clostridium cadaveris, and Clostridium senegalense respectively, while FS03 may represent a novel species of the genus Clostridium. Bioinformatics analysis using antiSMASH 5.0 predicted the presence of eight biosynthetic gene clusters (BGCs) encoding for the synthesis of ribosomally synthesized post-translationally modified peptides (RiPPs) and non-ribosomal peptides (NRPs) in four genomes. All predicted BGCs showed no similarity with any known BGCs suggesting novelty of the molecules from those predicted gene clusters. In addition, the analysis of genomes for putative virulence factors revealed the presence of four putative Clostridium toxin related genes in FS01 and FS2.2 genomes. No genes associated with the main Clostridium toxins were identified in the FS03 and FS04 genomes. Conclusions The presence of BGCs encoding for uncharacterized RiPPs and NRPSs in the genomes of antagonistic Clostridium spp. isolated from farm soil indicated their potential to produce novel secondary metabolites. This study serves as a basis for the identification and characterization of potent antimicrobials from these soil Clostridium spp. and expands the current knowledge base, encouraging future research into bioactive compound production in members of the genus Clostridium.https://doi.org/10.1186/s12864-021-08005-2Clostridium spp.AntimicrobialBiosynthesis gene clustersGenome miningRibosomally synthesized post-translationally modified peptidesNon-ribosomal peptides |
spellingShingle | Amila S. N. W. Pahalagedara Ruy Jauregui Paul Maclean Eric Altermann Steve Flint Jon Palmer Gale Brightwell Tanushree Barua Gupta Culture and genome-based analysis of four soil Clostridium isolates reveal their potential for antimicrobial production BMC Genomics Clostridium spp. Antimicrobial Biosynthesis gene clusters Genome mining Ribosomally synthesized post-translationally modified peptides Non-ribosomal peptides |
title | Culture and genome-based analysis of four soil Clostridium isolates reveal their potential for antimicrobial production |
title_full | Culture and genome-based analysis of four soil Clostridium isolates reveal their potential for antimicrobial production |
title_fullStr | Culture and genome-based analysis of four soil Clostridium isolates reveal their potential for antimicrobial production |
title_full_unstemmed | Culture and genome-based analysis of four soil Clostridium isolates reveal their potential for antimicrobial production |
title_short | Culture and genome-based analysis of four soil Clostridium isolates reveal their potential for antimicrobial production |
title_sort | culture and genome based analysis of four soil clostridium isolates reveal their potential for antimicrobial production |
topic | Clostridium spp. Antimicrobial Biosynthesis gene clusters Genome mining Ribosomally synthesized post-translationally modified peptides Non-ribosomal peptides |
url | https://doi.org/10.1186/s12864-021-08005-2 |
work_keys_str_mv | AT amilasnwpahalagedara cultureandgenomebasedanalysisoffoursoilclostridiumisolatesrevealtheirpotentialforantimicrobialproduction AT ruyjauregui cultureandgenomebasedanalysisoffoursoilclostridiumisolatesrevealtheirpotentialforantimicrobialproduction AT paulmaclean cultureandgenomebasedanalysisoffoursoilclostridiumisolatesrevealtheirpotentialforantimicrobialproduction AT ericaltermann cultureandgenomebasedanalysisoffoursoilclostridiumisolatesrevealtheirpotentialforantimicrobialproduction AT steveflint cultureandgenomebasedanalysisoffoursoilclostridiumisolatesrevealtheirpotentialforantimicrobialproduction AT jonpalmer cultureandgenomebasedanalysisoffoursoilclostridiumisolatesrevealtheirpotentialforantimicrobialproduction AT galebrightwell cultureandgenomebasedanalysisoffoursoilclostridiumisolatesrevealtheirpotentialforantimicrobialproduction AT tanushreebaruagupta cultureandgenomebasedanalysisoffoursoilclostridiumisolatesrevealtheirpotentialforantimicrobialproduction |