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Abstract

Bacterial secondary metabolites are crucial bioactive compounds with significant therapeutic potential, playing key roles in ecological processes and the discovery of novel antimicrobial agents and natural products. Cenotes, as extreme environments, harbour untapped microbial diversity and hold an interesting potential as sources of novel secondary metabolites. While research has focused on the fauna and flora of cenotes, the study of their microbial communities and their biosynthetic capabilities remains limited. Advances in metagenomics and genome sequencing have greatly improved the capacity to explore these communities and their metabolites. In this study, we analysed the microbial diversity and biotechnological potential of micro-organisms inhabiting sediments from a coastal cenote. Metagenomic analyses revealed a rich diversity of bacterial and archaeal communities, containing several novel biosynthetic gene clusters (BGCs) linked to secondary metabolite production. Notably, polyketide synthase BGCs, including those encoding ladderanes and aryl-polyenes, were identified. Bioinformatics analyses of these pathways suggest the presence of compounds with potential industrial and pharmaceutical applications. These findings highlight the biotechnological value of cenotes as reservoirs of secondary metabolites. The study and conservation of these ecosystems are essential to facilitate the discovery of new bioactive compounds that could benefit various industries.

Funding
This study was supported by the:
  • Consejo Nacional de Ciencia y Tecnología (Award 788622)
    • Principle Award Recipient: PerlaContreras-de la Rosa
  • Consejo Nacional de Ciencia y Tecnología (Award INFR-2016-01-269833)
    • Principle Award Recipient: AileenO´Connor-Sánchez
  • Consejo Nacional de Ciencia y Tecnología (Award A1-S-10785)
    • Principle Award Recipient: AlejandraPrieto-Davó
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2025-04-03
2025-04-27
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References

  1. Waters CM, Bassler BL. QUORUM SENSING: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 2005; 21:319–346 [View Article] [PubMed]
    [Google Scholar]
  2. Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 1994; 176:269–275 [View Article]
    [Google Scholar]
  3. West SA, Griffin AS, Gardner A, Diggle SP. Social evolution theory for microorganisms. Nat Rev Microbiol 2006; 4:597–607 [View Article] [PubMed]
    [Google Scholar]
  4. Williams P, Winzer K, Chan WC, Cámara M. Look who’s talking: communication and quorum sensing in the bacterial world. Philos Trans R Soc Lond B Biol Sci 2007; 362:1119–1134 [View Article] [PubMed]
    [Google Scholar]
  5. Diggle SP, Griffin AS, Campbell GS, West SA. Cooperation and conflict in quorum-sensing bacterial populations. Nature 2007; 450:411–414 [View Article] [PubMed]
    [Google Scholar]
  6. Ghoul M, Mitri S. The ecology and evolution of microbial competition. Trends Microbiol 2016; 24:833–845 [View Article] [PubMed]
    [Google Scholar]
  7. Dobson A, Cotter PD, Ross RP, Hill C. Bacteriocin production: a probiotic trait?. Appl Environ Microbiol 2012; 78:1–6 [View Article]
    [Google Scholar]
  8. Santos ALSD, Galdino ACM, Mello TPD, Ramos LDS, Branquinha MH et al. What are the advantages of living in a community? a microbial biofilm perspective!. Mem Inst Oswaldo Cruz 2018; 113:e180212 [View Article] [PubMed]
    [Google Scholar]
  9. Chung Y-H, Kim H, Ji C-H, Je H-W, Lee D et al. Comparative genomics reveals a remarkable biosynthetic potential of the Streptomyces phylogenetic lineage associated with rugose-ornamented spores. mSystems 2021; 6:e00489–21 [View Article]
    [Google Scholar]
  10. Ballouz S, Francis AR, Lan R, Tanaka MM. Conditions for the evolution of gene clusters in bacterial genomes. PLoS Comput Biol 2010; 6:e1000672 [View Article]
    [Google Scholar]
  11. Kramar A, Kostic MM. Bacterial secondary metabolites as biopigments for textile dyeing. Textiles 2022; 2:252–264 [View Article]
    [Google Scholar]
  12. Robinson J. Polyketide synthase com plexes: their structure and function in antibiotic biosynthesis. Phil Trans R Soc Lond B 1991; 332:107–114 [View Article]
    [Google Scholar]
  13. Mankelow DP, Neilan BA. Non-ribosomal peptide antibiotics. Expert Opin Ther Pat 2000; 10:1583–1591 [View Article]
    [Google Scholar]
  14. Bouazza F, Renoux B, Bachmann C, Gesson J-P. Total Synthesis and conformational analysis of the antifungal agent (−)-PF1163B. Org Lett 2003; 5:4049–4052 [View Article]
    [Google Scholar]
  15. Murphy AC, Corney M, Monson RE, Matilla MA, Salmond GPC et al. Biosynthesis of antifungal solanimycin may involve an iterative nonribosomal peptide synthetase module. ACS Chem Biol 2023; 18:1148–1157 [View Article] [PubMed]
    [Google Scholar]
  16. Piel J, Hui D, Fusetani N, Matsunaga S. Targeting modular polyketide synthases with iteratively acting acyltransferases from metagenomes of uncultured bacterial consortia. Environ Microbiol 2004; 6:921–927 [View Article] [PubMed]
    [Google Scholar]
  17. Agrawal S, Acharya D, Adholeya A, Barrow CJ, Deshmukh SK. Nonribosomal peptides from marine microbes and their antimicrobial and anticancer potential. Front Pharmacol 2017; 8:828 [View Article] [PubMed]
    [Google Scholar]
  18. Armando RG, Mengual Gómez DL, Gomez DE. New drugs are not enough‑drug repositioning in oncology: an update. Int J Oncol 2020; 56:651–684 [View Article] [PubMed]
    [Google Scholar]
  19. Huemer M, Mairpady Shambat S, Brugger SD, Zinkernagel AS. Antibiotic resistance and persistence-Implications for human health and treatment perspectives. EMBO Rep 2020; 21:e51034 [View Article] [PubMed]
    [Google Scholar]
  20. Sujatha P, Bapi Raju KVVSN, Ramana T. Studies on a new marine streptomycete BT-408 producing polyketide antibiotic SBR-22 effective against methicillin resistant Staphylococcus aureus. Microbiol Res 2005; 160:119–126 [View Article] [PubMed]
    [Google Scholar]
  21. Mohamed MF, Hamed MI, Panitch A, Seleem MN. Targeting methicillin-resistant Staphylococcus aureus with short salt-resistant synthetic peptides. Antimicrob Agents Chemother 2014; 58:4113–4122 [View Article] [PubMed]
    [Google Scholar]
  22. Katz L, Baltz RH. Natural product discovery: past, present, and future. J Ind Microbiol Biotechnol 2016; 43:155–176 [View Article] [PubMed]
    [Google Scholar]
  23. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol 1998; 5:R245–R249 [View Article]
    [Google Scholar]
  24. Mullis MM, Rambo IM, Baker BJ, Reese BK. Diversity, ecology, and prevalence of antimicrobials in nature. Front Microbiol 2019; 10:2518 [View Article] [PubMed]
    [Google Scholar]
  25. Zothanpuia, Passari AK, Leo VV, Chandra P, Kumar B et al. Bioprospection of actinobacteria derived from freshwater sediments for their potential to produce antimicrobial compounds. Microb Cell Fact 2018; 17:68 [View Article] [PubMed]
    [Google Scholar]
  26. Cuadrat RRC, Ionescu D, Dávila AMR, Grossart HP. Recovering genomics clusters of secondary metabolites from lakes using genome-resolved metagenomics. Front Microbiol 2018; 9:251 [View Article] [PubMed]
    [Google Scholar]
  27. Arroyave J, Martinez CM, Martínez‐Oriol FH, Sosa E, Alter SE. Regional‐scale aquifer hydrogeology as a driver of phylogeographic structure in the neotropical catfish Rhamdia guatemalensis (siluriformes: heptapteridae) from cenotes of the Yucatán Peninsula, Mexico. Freshw Biol 2021; 66:332–348 [View Article]
    [Google Scholar]
  28. Bauer-Gottwein P, Gondwe BRN, Charvet G, Marín LE, Rebolledo-Vieyra M et al. Review: The Yucatán Peninsula karst aquifer, Mexico. Hydrogeol J 2011; 19:507–524 [View Article]
    [Google Scholar]
  29. Schmitter-Soto JJ, Comín FA, Escobar-Briones E, Herrera-Silveira J, Alcocer J et al. Hydrogeochemical and biological characteristics of cenotes in the Yucatan Peninsula. Hydrobiologia 2002; 467:215–228 [View Article]
    [Google Scholar]
  30. Schmitter-Soto JJ, Escobar-Briones E, Alcocer J, Suárez-Morales E, Elías-Gutiérrez M et al. Los cenotes de la Península de Yucatán. In México AGT. ed Lagos y Presas de México 2002 https://www.researchgate.net/publication/228984086_Los_cenotes_de_la_Peninsula_de_Yucatan
    [Google Scholar]
  31. Polanco Rodríguez AG, Alberto JAN, Sánchez JS, Rejón GJM, Gómez JM et al. Contamination by organochlorine pesticides in the aquifer of the R ing of cenotes in yucatán, M éxico. Water Environ J 2015; 29:140–150
    [Google Scholar]
  32. Metcalfe CD, Beddows PA, Bouchot GG, Metcalfe TL, Li H et al. Contaminants in the coastal karst aquifer system along the caribbean coast of the Yucatan Peninsula, Mexico. Environ Pollut 2011; 159:991–997 [View Article] [PubMed]
    [Google Scholar]
  33. Ortega-Camacho D, Acosta-González G, Sánchez-Trujillo F, Cejudo E. Heavy metals in the sediments of urban sinkholes in Cancun, Quintana Roo. Sci Rep 2023; 13:7031 [View Article] [PubMed]
    [Google Scholar]
  34. Arcega‐Cabrera F, Sickman JO, Fargher L, Herrera‐Silveira J, Lucero D et al. Groundwater quality in the Yucatan Peninsula: insights from stable isotope and metals analysis. Groundwater 2021; 59:878–891 [View Article]
    [Google Scholar]
  35. León-Borges JA, Viveros-Jiménez F, Rodríguez-Mata AE, Lizardi-Jiménez MA. Hydrocarbon contamination patterns in the cenotes of the Mexican caribbean: the application of principal component analysis. Bull Environ Contam Toxicol 2020; 105:758–763 [View Article] [PubMed]
    [Google Scholar]
  36. Borbolla-Vazquez J, Ugalde-Silva P, León-Borges J, Díaz-Hernández JA. Total and faecal coliforms presence in cenotes of Cancun; Quintana Roo, Mexico. BioRisk 2020; 15:31–43 [View Article]
    [Google Scholar]
  37. Ritter SM, Isenbeck-Schröter M, Scholz C, Keppler F, Gescher J et al. Subaqueous speleothems (Hells Bells) formed by the interplay of pelagic redoxcline biogeochemistry and specific hydraulic conditions in the El Zapote sinkhole, Yucatán Peninsula, Mexico. Biogeosciences 2019; 16:2285–2305 [View Article]
    [Google Scholar]
  38. Stinnesbeck W, Frey E, Zell P, Avilés J, Hering F et al. Hells Bells – unique speleothems from the Yucatán Peninsula, Mexico, generated under highly specific subaquatic conditions. Palaeogeogr Palaeoclimatol Palaeoecol 2018; 489:209–229 [View Article]
    [Google Scholar]
  39. Adame MF, Santini NS, Torres-Talamante O, Rogers K. Mangrove sinkholes (cenotes) of the yucatan peninsula, a global hotspot of carbon sequestration. Biol Lett 2021; 17:20210037 [View Article] [PubMed]
    [Google Scholar]
  40. Scholz T, Vargas-Vázquez J, Moravec F, Vivas-Rodríguez C, Mendoza-Franco E. Cenotes (sinkholes) of the yucatan peninsula, mexico, as a habitat of adult trematodes of fish. Folia Parasitol 1995; 42:37–47
    [Google Scholar]
  41. Rivera Arriaga E, Suárez Morales E. Hidrología fauna acuática de los cenotes de la península de yucatán. revista de la sociedad mexicana de historia natural; 1998 http://repositorio.fciencias.unam.mx:8080/jspui/bitstream/11154/143136/1/48VHidrologia Fauna.pdf
  42. MacSwiney G. MC, Vilchis L. P, Clarke FM, Racey PA. The importance of cenotes in conserving bat assemblages in the Yucatan, Mexico. Biol Conserv 2007; 136:499–509 [View Article]
    [Google Scholar]
  43. MacSwiney G. MC, Bolívar Cimé B, Clarke FM, Racey PA. Insectivorous bat activity at cenotes in the Yucatan Peninsula, Mexico. Acta Chiropterologica 2009; 11:139–147 [View Article]
    [Google Scholar]
  44. Angyal DF, Chávez-Solís E, Liévano-Beltrán L, Simoes N. Quick identification guide to the subterranean fauna of the cenotes in the Yucatan Peninsula; 2021 https://zenodo.org/record/4661450 accessed 8 July 2024
  45. Vernes K, Devos F. Use of cenotes and the cave environment by mammals on the yucatán peninsula, Mexico. Biotropica 2022; 54:881–892 [View Article]
    [Google Scholar]
  46. Barba-Meinecke H, Arano Recio DE, Chávez AP. Archaeological evidence in the caves and cenotes of the Yucatán Peninsula, Mexico. In Underwater and Coastal Archaeology in Latin America University Press of Florida; 2023 pp 19–32 [View Article]
    [Google Scholar]
  47. López‐Martínez R, Solleiro‐Rebolledo E, Chávez‐Vergara B, Díaz‐Ortega J, Merino A et al. Early holocene charcoal accumulations in the Aktun Ha cenote: evidence of fire used by the first settlers of the Yucatán Peninsula, Mexico. Geoarchaeology 2020; 35:819–833 [View Article]
    [Google Scholar]
  48. Suárez-Moo P, Remes-Rodríguez CA, Márquez-Velázquez NA, Falcón LI, García-Maldonado JQ et al. Changes in the sediment microbial community structure of coastal and inland sinkholes of a karst ecosystem from the Yucatan peninsula. Sci Rep 2022; 12:1110 [View Article] [PubMed]
    [Google Scholar]
  49. Moore A, Lenczewski M, Leal-Bautista RM, Duvall M. Groundwater microbial diversity and antibiotic resistance linked to human population density in Yucatan Peninsula, Mexico. Can J Microbiol 2020; 66:46–58 [View Article] [PubMed]
    [Google Scholar]
  50. Brankovits D, Pohlman JW, Niemann H, Leigh MB, Leewis MC et al. Methane- and dissolved organic carbon-fueled microbial loop supports a tropical subterranean estuary ecosystem. Nat Commun 2017; 8:1835 [View Article] [PubMed]
    [Google Scholar]
  51. Stinnesbeck W, Frey E, Zell P, Avilés J, Hering F et al. Hells Bells – unique speleothems from the Yucatán Peninsula, Mexico, generated under highly specific subaquatic conditions. Palaeogeography, Palaeoclimatology, Palaeoecology 2018; 489:209–229 [View Article]
    [Google Scholar]
  52. Marfil-Santana MD, O’Connor-Sánchez A, Ramírez-Prado JH, De Los Santos-Briones C, López-Aguiar LK et al. A computationally simplistic poly-phasic approach to explore microbial communities from the Yucatan aquifer as A potential sources of novel natural products. J Microbiol 2016; 54:774–781 [View Article] [PubMed]
    [Google Scholar]
  53. Apolinar-Hernández MM, Peña-Ramírez YJ, Pérez-Rueda E, Canto-Canché BB, De Los Santos-Briones C et al. Identification and in silico characterization of two novel genes encoding peptidases S8 found by functional screening in a metagenomic library of yucatán underground water. Gene 2016; 593:154–161 [View Article] [PubMed]
    [Google Scholar]
  54. Góngora-Castillo E, López-Ochoa LA, Apolinar-Hernández MM, Caamal-Pech AM, Contreras-de la Rosa PA et al. Data mining of metagenomes to find novel enzymes: a non-computationally intensive method. 3 Biotech 2020; 10:78 [View Article] [PubMed]
    [Google Scholar]
  55. Suárez-Moo P, Prieto-Davó A. Biosynthetic potential of the sediment microbial subcommunities of an unexplored karst ecosystem and its ecological implications. Microbiologyopen 2024; 13:e1407 [View Article] [PubMed]
    [Google Scholar]
  56. Wissner JL, Parada-Fabián JC, Márquez-Velázquez NA, Escobedo-Hinojosa W, Gaudêncio SP et al. Diversity and bioprospection of gram-positive bacteria derived from a Mayan Sinkhole. Microb Ecol 2024; 87:77 [View Article] [PubMed]
    [Google Scholar]
  57. Andrews S. FastQC: una herramienta de control de calidad para datos de secuencia de alto rendimiento. n.d https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
  58. Keegan KP, Glass EM, Meyer F. MG-RAST, a Metagenomics Service for Analysis of Microbial Community Structure and Function. In Martin F, Uroz S. eds Microbial Environmental Genomics (MEG) [Internet] New York, NY: Springer New York; 2016 pp 207–233 [View Article]
    [Google Scholar]
  59. McMurdie PJ, Holmes S. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 2013; 8:e61217 [View Article] [PubMed]
    [Google Scholar]
  60. Li D, Liu CM, Luo R, Sadakane K, Lam TW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinform 2015; 31:1674–1676 [View Article] [PubMed]
    [Google Scholar]
  61. Kang DD, Froula J, Egan R, Wang Z. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 2015; 3:e1165 [View Article] [PubMed]
    [Google Scholar]
  62. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  63. Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol 2017; 35:725–731 [View Article] [PubMed]
    [Google Scholar]
  64. Chaumeil PA, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinform 2019; 36:1925–1927 [View Article] [PubMed]
    [Google Scholar]
  65. Community TG, Abueg LAL, Afgan E, Allart O, Awan AH et al. The galaxy platform for accessible, reproducible, and collaborative data analyses. Nucleic Acids Res 2024; 52:W83–W94
    [Google Scholar]
  66. Magurran AE. Ecological Diversity and Its Measurement Dordrecht: Springer Netherlands; 1988 [View Article]
    [Google Scholar]
  67. Oksanen J et al. Vegan: community ecology package. R package; 2022 https://cran.r-project.org/web/packages/vegan/vegan.pdf
  68. Bray JR, Curtis JT. An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 1957; 27:325–349 [View Article]
    [Google Scholar]
  69. Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP et al. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 2021; 49:W29–W35 [View Article] [PubMed]
    [Google Scholar]
  70. NCBI Resource Coordinators NCBI: National Center for Biotechnology Information. n.d https://www.ncbi.nlm.nih.gov/; Available from: https://www.ncbi.nlm.nih.gov/
  71. Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res 2023; 51:D587–D592 [View Article] [PubMed]
    [Google Scholar]
  72. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [View Article] [PubMed]
    [Google Scholar]
  73. Kautsar SA, van der Hooft JJJ, de Ridder D, Medema MH. BiG-SLiCE: A highly scalable tool maps the diversity of 1.2 million biosynthetic gene clusters. Gigascience 2021; 10:giaa154 [View Article] [PubMed]
    [Google Scholar]
  74. Kautsar SA, Blin K, Shaw S, Weber T, Medema MH. BiG-FAM: the biosynthetic gene cluster families database. Nucleic Acids Res 2021; 49:D490–D497 [View Article] [PubMed]
    [Google Scholar]
  75. Terlouw BR, Blin K, Navarro-Muñoz JC, Avalon NE, Chevrette MG et al. MIBiG 3.0: a community-driven effort to annotate experimentally validated biosynthetic gene clusters. Nucleic Acids Res 2023; 51:D603–D610 [View Article] [PubMed]
    [Google Scholar]
  76. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  77. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0; 2010 http://www.atgc-montpellier.fr/download/papers/phyml_2010.pdf
  78. Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
    [Google Scholar]
  79. Gómez-Acata ES, Teutli C, Falcón LI, García-Maldonado JQ, Prieto-Davó A et al. Sediment microbial community structure associated to different ecological types of mangroves in Celestún, a coastal lagoon in the Yucatan Peninsula, Mexico. PeerJ 2023; 11:e14587 [View Article] [PubMed]
    [Google Scholar]
  80. Barton LL, Fardeau ML, Fauque GD. Hydrogen sulfide: a toxic gas produced by dissimilatory sulfate and sulfur reduction and consumed by microbial oxidation. In Kroneck PMH, Torres MES. eds The Metal-Driven Biogeochemistry of Gaseous Compounds in the Environment [Internet] Dordrecht: Springer Netherlands; 2014 pp 237–277 [View Article]
    [Google Scholar]
  81. Muscarella ME, Boot CM, Broeckling CD, Lennon JT. Resource heterogeneity structures aquatic bacterial communities. ISME J 2019; 13:2183–2195 [View Article] [PubMed]
    [Google Scholar]
  82. Alonso-Sáez L, Gasol JM. Seasonal variations in the contributions of different bacterial groups to the uptake of low-molecular-weight compounds in northwestern mediterranean coastal waters. Appl Environ Microbiol 2007; 73:3528–3535 [View Article] [PubMed]
    [Google Scholar]
  83. Gómez-Consarnau L, Lindh MV, Gasol JM, Pinhassi J. Structuring of bacterioplankton communities by specific dissolved organic carbon compounds. Environ Microbiol 2012; 14:2361–2378 [View Article] [PubMed]
    [Google Scholar]
  84. Zhou Y, Kellermann C, Griebler C. Spatio-temporal patterns of microbial communities in a hydrologically dynamic pristine aquifer. FEMS Microbiol Ecol 2012; 81:230–242 [View Article] [PubMed]
    [Google Scholar]
  85. Kim B-R, Shin J, Guevarra R, Lee JH, Kim DW et al. Deciphering diversity indices for a better understanding of microbial communities. J Microbiol Biotechnol 2017; 27:2089–2093 [View Article] [PubMed]
    [Google Scholar]
  86. Campbell TP, Ulrich DEM, Toyoda J, Thompson J, Munsky B et al. Microbial Communities Influence Soil dissolved organic carbon concentration by altering metabolite composition. Front Microbiol 2021; 12:799014 [View Article] [PubMed]
    [Google Scholar]
  87. Li D, Sharp JO, Saikaly PE, Ali S, Alidina M et al. Dissolved organic carbon influences microbial community composition and diversity in managed aquifer recharge systems. Appl Environ Microbiol 2012; 78:6819–6828 [View Article] [PubMed]
    [Google Scholar]
  88. Wei B, Du A-Q, Zhou Z-Y, Lai C, Yu W-C et al. An atlas of bacterial secondary metabolite biosynthesis gene clusters. Environ Microbiol 2021; 23:6981–6992 [View Article] [PubMed]
    [Google Scholar]
  89. Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2017; 2:1533–1542 [View Article]
    [Google Scholar]
  90. Singh NK, Wood JM, Patane J, Moura LMS, Lombardino J et al. Characterization of metagenome-assembled genomes from the international space station. Microbiome 2023; 11:125 [View Article] [PubMed]
    [Google Scholar]
  91. Blin K, Kim HU, Medema MH, Weber T. Recent development of antiSMASH and other computational approaches to mine secondary metabolite biosynthetic gene clusters. Brief Bioinform 2019; 20:1103–1113 [View Article] [PubMed]
    [Google Scholar]
  92. Schöner TA, Gassel S, Osawa A, Tobias NJ, Okuno Y et al. Aryl Polyenes, a highly abundant class of bacterial natural products, are functionally related to antioxidative carotenoids. Chembiochem 2016; 17:247–253 [View Article] [PubMed]
    [Google Scholar]
  93. Johnston I, Osborn LJ, Markley RL, McManus EA, Kadam A et al. Identification of essential genes for Escherichia coli aryl polyene biosynthesis and function in biofilm formation. NPJ Biofilms Microbiomes 2021; 7:56 [View Article] [PubMed]
    [Google Scholar]
  94. Rajagopal L, Sundari CS, Balasubramanian D, Sonti RV. The bacterial pigment xanthomonadin offers protection against photodamage. FEBS Lett 1997; 415:125–128 [View Article] [PubMed]
    [Google Scholar]
  95. Poplawsky AR, Urban SC, Chun W. Biological role of xanthomonadin pigments in xanthomonas campestris pv. Campestris 2000; 66:5123–5127 [View Article]
    [Google Scholar]
  96. Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 2013; 11:443–454 [View Article]
    [Google Scholar]
  97. Zhao X, Drlica K. Reactive oxygen species and the bacterial response to lethal stress. Curr Opin Microbiol 2014; 21:1–6 [View Article] [PubMed]
    [Google Scholar]
  98. Dragoš A, Andersen AJC, Lozano-Andrade CN, Kempen PJ, Kovács ÁT et al. Phages carry interbacterial weapons encoded by biosynthetic gene clusters. Current Biology 2021; 31:3479–3489 [View Article]
    [Google Scholar]
  99. Achudhan AB, Kannan P, Saleena LM. CRISPR detection in metagenome-assembled genomes (MAGs) of coal mine. Funct Integr Genomics 2023; 23:122 [View Article] [PubMed]
    [Google Scholar]
  100. Robinson SL, Christenson JK, Wackett LP. Biosynthesis and chemical diversity of β-lactone natural products. Nat Prod Rep 2019; 36:458–475 [View Article]
    [Google Scholar]
  101. Schröter MA, Meyer S, Hahn MB, Solomun T, Sturm H et al. Ectoine protects DNA from damage by ionizing radiation. Sci Rep 2017; 7:15272 [View Article] [PubMed]
    [Google Scholar]
  102. Salvador M, Argandoña M, Naranjo E, Piubeli F, Nieto JJ et al. Quantitative RNA-seq analysis unveils osmotic and thermal adaptation mechanisms relevant for ectoine production in Chromohalobacter salexigens. Front Microbiol 2018; 9:1845 [View Article] [PubMed]
    [Google Scholar]
  103. Gunde-Cimerman N, Plemenitaš A, Oren A. Strategies of adaptation of microorganisms of the three domains of life to high salt concentrations. FEMS Microbiology Reviews 2018; 42:353–375 [View Article]
    [Google Scholar]
  104. Kolp S, Pietsch M, Galinski EA, Gütschow M. Compatible solutes as protectants for zymogens against proteolysis. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 2006; 1764:1234–1242 [View Article]
    [Google Scholar]
  105. van Teeseling MCF, Neumann S, van Niftrik L. The anammoxosome organelle is crucial for the energy metabolism of anaerobic ammonium oxidizing bacteria. Microb Physiol 2013; 23:104–117 [View Article]
    [Google Scholar]
  106. van Niftrik L, Jetten MSM. Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 2012; 76:585–596 [View Article] [PubMed]
    [Google Scholar]
  107. Kartal B, van Niftrik L, Keltjens JT, Op den Camp HJM, Jetten MSM. Anammox--growth physiology, cell biology, and metabolism. Adv Microb Physiol 2012; 60:211–262 [View Article] [PubMed]
    [Google Scholar]
  108. Javidpour P, Deutsch S, Mutalik VK, Hillson NJ, Petzold CJ et al. Investigation of proposed ladderane biosynthetic genes from anammox bacteria by heterologous expression in E. coli. PLoS One 2016; 11:e0151087 [View Article] [PubMed]
    [Google Scholar]
  109. Choudoir MJ, Pepe-Ranney C, Buckley DH. Diversification of secondary metabolite biosynthetic gene clusters coincides with lineage divergence in streptomyces. Antibiotics 2018; 7:12 [View Article] [PubMed]
    [Google Scholar]
  110. Sharrar AM, Crits-Christoph A, Méheust R, Diamond S, Starr EP et al. Bacterial secondary metabolite biosynthetic potential in soil varies with phylum, depth, and vegetation type. mBio 2020; 11:e00416-20 [View Article] [PubMed]
    [Google Scholar]
  111. Geller-McGrath D, Mara P, Taylor GT, Suter E, Edgcomb V et al. Diverse secondary metabolites are expressed in particle-associated and free-living microorganisms of the permanently anoxic cariaco basin. Nat Commun 2023; 14:656 [View Article] [PubMed]
    [Google Scholar]
  112. Rattray JE, Strous M, Op den Camp HJ, Schouten S, Jetten MS et al. A comparative genomics study of genetic products potentially encoding ladderane lipid biosynthesis. Biol Direct 2009; 4:8 [View Article]
    [Google Scholar]
  113. Süssmuth RD, Mainz A. Nonribosomal peptide synthesis—principles and prospects. Angew Chem Int Ed 2017; 56:3770–3821 [View Article]
    [Google Scholar]
  114. Murphy R, Strube ML, Schmidt S, Silué KS, Koné NA et al. Non-ribosomal peptide synthase profiles remain structurally similar despite minimally shared features across fungus-farming termite microbiomes. ISME Commun 2024; 4:ycae094 [View Article] [PubMed]
    [Google Scholar]
  115. Zan J, Li Z, Tianero MaD, Davis J, Hill RT et al. A microbial factory for defensive kahalalides in a tripartite marine symbiosis. Science 2019; 364:eaaw6732 [View Article]
    [Google Scholar]
  116. Li R, Shi H, Zhao X, Liu X, Duan Q et al. Development and application of an efficient recombineering system for burkholderia glumae and burkholderia plantarii. Microb Biotechnol 2021; 14:1809–1826 [View Article] [PubMed]
    [Google Scholar]
  117. Esmaeel Q, Pupin M, Kieu NP, Chataigné G, Béchet M et al. Burkholderia genome mining for nonribosomal peptide synthetases reveals a great potential for novel siderophores and lipopeptides synthesis. Microbiologyopen 2016; 5:512–526 [View Article] [PubMed]
    [Google Scholar]
  118. Bach E, Passaglia LMP, Jiao J, Gross H. Burkholderia in the genomic era: from taxonomy to the discovery of new antimicrobial secondary metabolites. Crit Rev Microbiol 2022; 48:121–160 [View Article] [PubMed]
    [Google Scholar]
  119. Alam K, Islam MM, Gong K, Abbasi MN, Li R et al. In silico genome mining of potential novel biosynthetic gene clusters for drug discovery from Burkholderia bacteria. Comput Biol Med 2022; 140:105046 [View Article] [PubMed]
    [Google Scholar]
  120. Waschulin V, Borsetto C, James R, Newsham KK, Donadio S et al. Biosynthetic potential of uncultured antarctic soil bacteria revealed through long-read metagenomic sequencing. ISME J 2022; 16:101–111 [View Article] [PubMed]
    [Google Scholar]
  121. Murray AE, Lo C-C, Daligault HE, Avalon NE, Read RW et al. Discovery of an antarctic ascidian-associated uncultivated Verrucomicrobia with antimelanoma palmerolide biosynthetic potential. mSphere 2021; 6:e00759–21 [View Article]
    [Google Scholar]
  122. Funk MA, van der Donk WA. Ribosomal natural products, tailored to fit. Acc Chem Res 2017; 50:1577–1586 [View Article] [PubMed]
    [Google Scholar]
  123. Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 2013; 30:108–160 [View Article] [PubMed]
    [Google Scholar]
  124. Li Y, Rebuffat S. The manifold roles of microbial ribosomal peptide-based natural products in physiology and ecology. J Biol Chem 2020; 295:34–54 [View Article] [PubMed]
    [Google Scholar]
  125. Liras P, Martín JF. Streptomyces clavuligerus: the omics era. J Ind Microbiol Biotechnol 2021; 48:kuab072 [View Article] [PubMed]
    [Google Scholar]
  126. Avalos M, Garbeva P, Vader L, van Wezel GP, Dickschat JS et al. Biosynthesis, evolution and ecology of microbial terpenoids. Nat Prod Rep 2022; 39:249–272 [View Article] [PubMed]
    [Google Scholar]
  127. Gershenzon J, Dudareva N. The function of terpene natural products in the natural world. Nat Chem Biol 2007; 3:408–414 [View Article]
    [Google Scholar]
  128. Reddy GK, Leferink NGH, Umemura M, Ahmed ST, Breitling R et al. Exploring novel bacterial terpene synthases. PLoS One 2020; 15:e0232220 [View Article] [PubMed]
    [Google Scholar]
  129. Chen X, Köllner TG, Jia Q, Norris A, Santhanam B et al. Terpene synthase genes in eukaryotes beyond plants and fungi: occurrence in social amoebae. Proc Natl Acad Sci USA 2016; 113:12132–12137 [View Article]
    [Google Scholar]
  130. Jiang M, Wu Z, Guo H, Liu L, Chen S. A review of terpenes from marine-derived fungi: 2015-2019. Mar Drugs 2020; 18:321 [View Article] [PubMed]
    [Google Scholar]
  131. Chen R, Wong HL, Kindler GS, MacLeod FI, Benaud N et al. Discovery of an abundance of biosynthetic gene clusters in shark bay microbial mats. Front Microbiol 2020; 11:1950 [View Article] [PubMed]
    [Google Scholar]
  132. Engene N, Rottacker EC, Kaštovský J, Byrum T, Choi H et al. Moorea producens gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. Int J Syst Evol Microbiol 2012; 62:1171–1178 [View Article] [PubMed]
    [Google Scholar]
  133. Ozaki T, Sugiyama R, Shimomura M, Nishimura S, Asamizu S et al. Identification of the common biosynthetic gene cluster for both antimicrobial streptoaminals and antifungal 5-alkyl-1,2,3,4-tetrahydroquinolines. Org Biomol Chem 2019; 17:2370–2378 [View Article]
    [Google Scholar]
  134. Touray M, Cimen H, Bode E, Bode HB, Hazir S. Effects of xenorhabdus and photorhabdus bacterial metabolites on the ovipositional activity of aedes albopictus. J Pest Sci 2024; 97:2203–2215 [View Article]
    [Google Scholar]
  135. Krithika VP, Bellie A, Shandeep G, Settu V, Thirunavukkarasu D et al. Genome mining of photorhabdus luminescens tnau1 reveals novel gene assets with insecticidal and nematicidal properties. Physiol Mol Plant Pathol 2024; 133:102358 [View Article]
    [Google Scholar]
  136. Tizard IR. Fish vaccines. In Vaccines for Veterinarians Elsevier; 2021 pp 281–292 [View Article]
    [Google Scholar]
  137. Marti T, Hu Z, Pohl NL, Shah AN, Khosla C. Cloning, nucleotide sequence, and heterologous expression of the biosynthetic gene cluster for R1128, a non-steroidal estrogen receptor antagonist. Insights into an unusual priming mechanism. J Biol Chem 2000; 275:33443–33448 [View Article] [PubMed]
    [Google Scholar]
  138. Räty K, Kantola J, Hautala A, Hakala J, Ylihonko K et al. Cloning and characterization of Streptomyces galilaeus aclacinomycins polyketide synthase (PKS) cluster. Gene 2002; 293:115–122 [View Article] [PubMed]
    [Google Scholar]
  139. Ramos A, Lombó F, Braña AF, Rohr J, Méndez C et al. Biosynthesis of elloramycin in Streptomyces olivaceus requires glycosylation by enzymes encoded outside the aglycon cluster. Microbiol 2008; 154:781–788 [View Article] [PubMed]
    [Google Scholar]
  140. Iqbal HA, Low-Beinart L, Obiajulu JU, Brady SF. Natural Product Discovery through improved functional metagenomics in Streptomyces. J Am Chem Soc 2016; 138:9341–9344 [View Article]
    [Google Scholar]
  141. Li Z, Huang Y, Dong F, Li W, Ding L et al. Swainsonine promotes apoptosis in human oesophageal squamous cell carcinoma cells in vitro and in vivo through activation of mitochondrial pathway. J Biosci 2012; 37:1005–1016 [View Article]
    [Google Scholar]
  142. Sun JY, Zhu MZ, Wang SW, Miao S, Xie YH et al. Inhibition of the growth of human gastric carcinoma in vivo and in vitro by swainsonine. Phytomedicine 2007; 14:353–359 [View Article]
    [Google Scholar]
  143. Sun J-Y, Yang H, Miao S, Li J-P, Wang S-W et al. Suppressive effects of swainsonine on C6 glioma cell in vitro and in vivo. Phytomedicine 2009; 16:1070–1074 [View Article] [PubMed]
    [Google Scholar]
  144. Li Z, Xu X, Huang Y, Ding L, Wang Z et al. Swainsonine activates mitochondria-mediated apoptotic pathway in human lung cancer A549 cells and retards the growth of lung cancer xenografts. Int J Biol Sci 2012; 8:394–405 [View Article] [PubMed]
    [Google Scholar]
  145. Cook D, Donzelli BGG, Creamer R, Baucom DL, Gardner DR et al. Swainsonine biosynthesis genes in diverse symbiotic and pathogenic fungi. G3 2017; 7:1791–1797 [View Article] [PubMed]
    [Google Scholar]
  146. Reveglia P, Masi M, Evidente A. Melleins-intriguing natural compounds. Biomolecules 2020; 10:772 [View Article] [PubMed]
    [Google Scholar]
  147. Rock CO. Fatty acid and phospholipid metabolism in prokaryotes. In Biochemistry of Lipids, Lipoproteins and Membranes Elsevier; pp 59–96 [View Article]
    [Google Scholar]
  148. Sul HS, Smith S. Fatty acid synthesis in eukaryotes. In Biochemistry of Lipids, Lipoproteins, and Membranes Elsevier; 2008 pp 155–190 [View Article]
    [Google Scholar]
  149. Chen A, Re RN, Burkart MD. Type II fatty acid and polyketide synthases: deciphering protein–protein and protein–substrate interactions. Nat Prod Rep 2018; 35:1029–1045 [View Article]
    [Google Scholar]
  150. Sulpizio A, Crawford CEW, Koweek RS, Charkoudian LK. Probing the structure and function of acyl carrier proteins to unlock the strategic redesign of type II polyketide biosynthetic pathways. J Biol Chem 2021; 296:100328 [View Article] [PubMed]
    [Google Scholar]
  151. Hertweck C, Luzhetskyy A, Rebets Y, Bechthold A. Type II polyketide synthases: gaining a deeper insight into enzymatic teamwork. Nat Prod Rep 2007; 24:162–190 [View Article]
    [Google Scholar]
  152. Kruth S, Nett M. n.d. Aurachins, bacterial antibiotics interfering with electron transport processes. Antibiotics 12:1067 [View Article]
    [Google Scholar]
  153. Kunze B, Höfle G, Reichenbach H. The aurachins, new quinoline antibiotics from myxobacteria : production, physico-chemical and biological properties. J Antibiot 1987; 40:258–265 [View Article]
    [Google Scholar]
  154. Pistorius D, Li Y, Sandmann A, Müller R. Completing the puzzle of aurachin biosynthesis in stigmatella aurantiaca Sg a15. Mol Biosyst 2011; 7:3308–3315 [View Article] [PubMed]
    [Google Scholar]
  155. Sandmann A, Dickschat J, Jenke-Kodama H, Kunze B, Dittmann E et al. A Type II polyketide synthase from the gram-negative bacterium stigmatella aurantiaca is involved in aurachin alkaloid biosynthesis. Angew Chem Int Ed Engl 2007; 46:2712–2716 [View Article] [PubMed]
    [Google Scholar]
  156. Cronan JE. Biotin and lipoic acid: synthesis, attachment, and regulation. EcoSal Plus 2014; 6: [View Article]
    [Google Scholar]
  157. Lin S, Hanson RE, Cronan JE. Biotin synthesis begins by hijacking the fatty acid synthetic pathway. Nat Chem Biol 2010; 6:682–688 [View Article] [PubMed]
    [Google Scholar]
  158. Byers DM, Gong H. Acyl carrier protein: structure-function relationships in a conserved multifunctional protein family. Biochem Cell Biol 2007; 85:649–662 [View Article] [PubMed]
    [Google Scholar]
  159. Khersonsky O, Tawfik DS. Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu Rev Biochem 2010; 79:471–505 [View Article] [PubMed]
    [Google Scholar]
  160. Peracchi A. The limits of enzyme specificity and the evolution of metabolism. Trends Biochem Sci 2018; 43:984–996 [View Article] [PubMed]
    [Google Scholar]
  161. Fischbach MA, Clardy J. One pathway, many products. Nat Chem Biol 2007; 3:353–355 [View Article] [PubMed]
    [Google Scholar]
  162. Wu Y, Seyedsayamdost MR. Synergy and target promiscuity drive structural divergence in bacterial alkylquinolone biosynthesis. Cell Chem Biol 2017; 24:1437–1444 [View Article] [PubMed]
    [Google Scholar]
  163. Martinet L, Naômé A, Deflandre B, Maciejewska M, Tellatin D et al. A single biosynthetic gene cluster is responsible for the production of bagremycin antibiotics and ferroverdin iron chelators. mBio 2019; 10:e01230-19 [View Article] [PubMed]
    [Google Scholar]
  164. Lee WC, Choi S, Jang A, Son K, Kim Y. Structural comparison of acinetobacter baumannii β-ketoacyl-acyl carrier protein reductases in fatty acid and aryl polyene biosynthesis. Sci Rep 2021; 11:7945 [View Article] [PubMed]
    [Google Scholar]
  165. Mukherjee A, Tikariha H, Bandla A, Pavagadhi S, Swarup S. Global analyses of biosynthetic gene clusters in phytobiomes reveal strong phylogenetic conservation of terpenes and aryl polyenes. mSystems 2023; 8:e0038723 [View Article] [PubMed]
    [Google Scholar]
  166. Nouri D, Tantillo D. They came from the deep: syntheses, applications, and biology of ladderanes. Curr Org Chem 2006; 10:2055–2074 [View Article]
    [Google Scholar]
  167. Caceres-Martinez LE, Saavedra Lopez J, Dagle RA, Gillespie R, Kenttämaa HI et al. Influence of blending cycloalkanes on the energy content, density, and viscosity of Jet-A. Fuel 2024; 358:129986 [View Article]
    [Google Scholar]
  168. Peixoto RS, Voolstra CR, Sweet M, Duarte CM, Carvalho S et al. Harnessing the microbiome to prevent global biodiversity loss. Nat Microbiol 2022; 7:1726–1735 [View Article]
    [Google Scholar]
  169. Averill C, Anthony MA, Baldrian P, Finkbeiner F, van den Hoogen J et al. Defending earth’s terrestrial microbiome. Nat Microbiol 2022; 7:1717–1725 [View Article] [PubMed]
    [Google Scholar]
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