1887

Microbiology Society logo

Volume 165, Issue 11

Awakening ancient polar : diversity, evolution and specialized metabolite potential Open Access

Abstract

Polar and subpolar ecosystems are highly vulnerable to global climate change with consequences for biodiversity and community composition. Bacteria are directly impacted by future environmental change and it is therefore essential to have a better understanding of microbial communities in fluctuating ecosystems. Exploration of Polar environments, specifically sediments, represents an exciting opportunity to uncover bacterial and chemical diversity and link this to ecosystem and evolutionary parameters. In terms of specialized metabolite production, the bacterial order , within the phylum are unsurpassed, producing 10 000 specialized metabolites accounting for over 45 % of all bioactive microbial metabolites. A selective isolation approach focused on spore-forming of 12 sediment cores from the Antarctic and sub-Arctic generated a culture collection of 50 strains. This consisted of 39 strains belonging to rare genera including and . This study used a combination of nanopore sequencing and molecular networking to explore the community composition, culturable bacterial diversity, evolutionary relatedness and specialized metabolite potential of these strains. Metagenomic analyses using MinION sequencing was able to detect the phylum across polar sediment cores at an average of 13 % of the total bacterial reads. The resulting molecular network consisted of 1652 parent ions and the lack of known metabolite identification supports the argument that Polar bacteria are likely to produce previously unreported chemistry.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Actinobacteria , Antarctic , Arctic , evolution , marine and specialized metabolites
© 2019 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000845
2019-11-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/165/11/1169.html?itemId=/content/journal/micro/10.1099/mic.0.000845&mimeType=html&fmt=ahah

References

  1. Newman DJ, Cragg GM. Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 2016; 79:629–661 [View Article]
     [Google Scholar]
  2. Bérdy J. Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot 2012; 65:385–395 [View Article]
     [Google Scholar]
  3. Qin Z, Munnoch JT, Devine R, Holmes NA, Seipke RF et al. Formicamycins, antibacterial polyketides produced by Streptomyces formicae isolated from African Tetraponera plant-ants. Chem Sci 2017; 8:3218–3227 [View Article]
     [Google Scholar]
  4. Seipke RF. Strain-level diversity of secondary metabolism in Streptomyces albus. PLoS One 2015; 10:e0116457–14 [View Article]
     [Google Scholar]
  5. Bérdy J. Bioactive microbial metabolites. J Antibiot 2005; 58:1–26 [View Article]
     [Google Scholar]
  6. Baltz RH. Marcel Faber roundtable: is our antibiotic pipeline unproductive because of starvation, constipation or lack of inspiration?. J Ind Microbiol Biotechnol 2006; 33:507–513 [View Article]
     [Google Scholar]
  7. Lazzarini A, Cavaletti L, Toppo G, Marinelli F. Rare genera of actinomycetes as potential producers of new antibiotics. Antonie van Leeuwenhoek 2000; 78:399–405 [View Article]
     [Google Scholar]
  8. Schorn MA, Alanjary MM, Aguinaldo K, Korobeynikov A, Podell S et al. Sequencing rare marine actinomycete genomes reveals high density of unique natural product biosynthetic gene clusters. Microbiology 2016; 162:2075–2086 [View Article]
     [Google Scholar]
  9. Jensen PR, Mafnas C. Biogeography of the marine actinomycete Salinispora. Environ Microbiol 2006; 8:1881–1888 [View Article]
     [Google Scholar]
  10. Tian XP, Long L-J, Li S-M, Zhang J, Xu Y et al. Pseudonocardia antitumoralis sp. nov., a deoxynyboquinone-producing actinomycete isolated from a deep-sea sediment. Int J Syst Evol Microbiol 2013; 63:893–899 [View Article]
     [Google Scholar]
  11. Gerwick WH, Moore BS. Lessons from the past and charting the future of marine natural products drug discovery and chemical biology. Chem Biol 2012; 19:85–98 [View Article]
     [Google Scholar]
  12. Maloney KN, Macmillan JB, Kauffman CA, Jensen PR, Dipasquale AG et al. Lodopyridone, a structurally unprecedented alkaloid from a marine actinomycete. Org Lett 2009; 11:5422–5424 [View Article]
     [Google Scholar]
  13. Pérez-Bonilla M, Oves-Costales D, de la Cruz M, Kokkini M, Martín J et al. Phocoenamicins B and C, new antibacterial Spirotetronates isolated from a marine Micromonospora sp. Mar Drugs 2018; 16:95–13 [View Article]
     [Google Scholar]
  14. Makhalanyane TP, Van Goethem MW, Cowan DA. Microbial diversity and functional capacity in polar soils. Curr Opin Biotechnol 2016; 38:159–166 [View Article]
     [Google Scholar]
  15. Zhang G, Cao T, Ying J, Yang Y, Ma L. Diversity and novelty of actinobacteria in Arctic marine sediments. Antonie van Leeuwenhoek 2014; 105:743–754 [View Article]
     [Google Scholar]
  16. Howe JA, Shimmield TM, Diaz R. Deep-Water sedimentary environments of the northwestern weddell sea and south sandwich islands, antarctica. Deep Sea Research Part II 2004; 51:1489–1514 [View Article]
     [Google Scholar]
  17. Howe JA, Shimmield TM, Harland R. Late quaternary contourites and glaciomarine sedimentation in the Fram Strait. Sedimentology 2008; 55:179–200
     [Google Scholar]
  18. Jorgensen SL, Hannisdal B. Correlating microbial community profiles with geochemical data in highly stratified sediments from the arctic mid-ocean ridge. Proc Natl Acad Sci USA 2012
     [Google Scholar]
  19. González-Rocha G, Muñoz-Cartes G, Canales-Aguirre CB, Lima CA, Domínguez-Yévenes M et al. Diversity structure of culturable bacteria isolated from the fildes peninsula (King George Island, Antarctica): a phylogenetic analysis perspective. PLoS One 2017; 12:e0179390–18 [View Article]
     [Google Scholar]
  20. Bienhold C, Boetius A, Ramette A. The energy-diversity relationship of complex bacterial communities in Arctic deep-sea sediments. ISME J 2012; 6:724–732 [View Article]
     [Google Scholar]
  21. Carr SA, Orcutt BN, Mandernack KW, Spear JR. Abundant atribacteria in deep marine sediment from the adélie basin, antarctica. Front Microbiol 2015; 6:403–412 [View Article]
     [Google Scholar]
  22. Yuan M, Yu Y, Li H-R, Dong N, Zhang X-H. Phylogenetic diversity and biological activity of actinobacteria isolated from the chukchi shelf marine sediments in the arctic ocean. Mar Drugs 2014; 12:1281–1297 [View Article]
     [Google Scholar]
  23. Purves K, Macintyre L, Brennan D, Hreggviðsson G, Kuttner E et al. Using molecular networking for microbial secondary metabolite Bioprospecting. Metabolites 2016; 6:2–18 [View Article]
     [Google Scholar]
  24. Mincer TJ, Jensen PR, Kauffman CA, Fenical W. Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 2002; 68:5005–5011 [View Article]
     [Google Scholar]
  25. Mohseni M, Norouzi H, Hamedi J, Roohi A. Screening of antibacterial producing actinomycetes from sediments of the Caspian sea. Int J Mol Cell Med 2013; 2:64–71
     [Google Scholar]
  26. Eden PA, Schmidt TM, Blakemore RP, Pace NR. Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. Int J Syst Bacteriol 1991; 41:324–325 [View Article]
     [Google Scholar]
  27. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article]
     [Google Scholar]
  28. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically United database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article]
     [Google Scholar]
  29. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article]
     [Google Scholar]
  30. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690 [View Article]
     [Google Scholar]
  31. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES science gateway for inference of large phylogenetic trees. gateway computing environments workshop (GCE). IEEE 20101–8
     [Google Scholar]
  32. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol 1966; 16:313–340 [View Article]
     [Google Scholar]
  33. Macintyre L, Zhang T, Viegelmann C, Martinez IJ, Cheng C et al. Metabolomic tools for secondary metabolite discovery from marine microbial symbionts. Mar Drugs 2014; 12:3416–3448 [View Article]
     [Google Scholar]
  34. Deutsch EW, Mendoza L, Shteynberg D, Farrah T, Lam H. A guided tour of the Trans-Proteomic Pipeline. In Martens L, Hermjakob H. (editors) Proteomics 10 2010 pp 1150–1159
     [Google Scholar]
  35. Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N et al. Sharing and community curation of mass spectrometry data with global natural products social molecular networking. Nature 2016; 34:828–837
     [Google Scholar]
  36. Smoot M, Ono K, Ideker T, Maere S. PiNGO: a Cytoscape plugin to find candidate genes in biological networks. Bioinformatics 2011; 27:1030–1031 [View Article]
     [Google Scholar]
  37. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2007; 2:2366–2382 [View Article]
     [Google Scholar]
  38. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM et al. The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 2008; 9:386–388 [View Article]
     [Google Scholar]
  39. Hanson NW, Konwar KM, Hawley AK, Altman T, Karp PD et al. Metabolic pathways for the whole community. BMC Genomics 2014; 15:619–14 [View Article]
     [Google Scholar]
  40. Stackebrandt E. Taxonomic parameters revisited: tarnished gold standards. Microbiology. Today 2006; 33:152–155
     [Google Scholar]
  41. Wicke C, Hüners M, Wray V, Nimtz M, Bilitewski U et al. Production and structure elucidation of glycoglycerolipids from a marine sponge-associated Microbacterium species. J Nat Prod 2000; 63:621–626 [View Article]
     [Google Scholar]
  42. Fusetani N, Hashimoto Y. Structures of two water soluble hemolysins isolated from the green alga Ulva pertusa. Agricultural and Biological Chemistry 1975; 39:2021–2025
     [Google Scholar]
  43. Fenical W, Jensen PR. Developing a new resource for drug discovery: marine actinomycete bacteria. Nat Chem Biol 2006; 2:666–673 [View Article]
     [Google Scholar]
  44. Jensen PR, Moore BS, Fenical W. The marine actinomycete genus Salinispora: a model organism for secondary metabolite discovery. Nat Prod Rep 2015; 32:738–751 [View Article]
     [Google Scholar]
  45. Holmes NA, Innocent TM, Heine D, Bassam MA, Worsley SF et al. Genome analysis of two Pseudonocardia phylotypes associated with Acromyrmex leafcutter ants reveals their biosynthetic potential. Front Microbiol 2016; 7:4307–4316 [View Article]
     [Google Scholar]
  46. Trujillo ME, Idris H, Riesco R, Nouioui I, Igual JM et al. Pseudonocardia nigra sp. nov., isolated from Atacama desert rock. Int J Syst Evol Microbiol 2017; 67:2980–2985 [View Article]
     [Google Scholar]
  47. Chen HH, Qin S, Li J, Zhang YQ, Xu LH et al. Pseudonocardia endophytica sp. nov., isolated from the pharmaceutical plant Lobelia clavata. Int J Syst Evol Microbiol 2009; 59:559–563 [View Article]
     [Google Scholar]
  48. Prabahar V, Dube S, Reddy GSN, Shivaji S. Pseudonocardia antarctica sp. nov. an actinomycetes from McMurdo dry Valleys, Antarctica. Syst Appl Microbiol 2004; 27:66–71 [View Article]
     [Google Scholar]
  49. Zhang DF, Jiang Z, Li L, Liu BB, Zhang XM et al. Pseudonocardia sediminis sp. nov., isolated from marine sediment. Int J Syst Evol Microbiol 2014; 64:745–750 [View Article]
     [Google Scholar]
  50. Zhao GZ, Zhu WY, Li J, Xie Q, Xu LH et al. Pseudonocardia serianimatus sp. nov., a novel actinomycete isolated from the surface-sterilized leaves of Artemisia annua L. Antonie van Leeuwenhoek 2011; 100:521–528 [View Article]
     [Google Scholar]
  51. Stackebrandt E, Goebel BM. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Evol Microbiol 1994; 44:846–849 [View Article]
     [Google Scholar]
  52. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article]
     [Google Scholar]
  53. Rossi-Tamisier M, Benamar S, Raoult D, Fournier PE. Cautionary tale of using 16S rRNA gene sequence similarity values in identification of human-associated bacterial species. Int J Syst Evol Microbiol 2015; 65:1929–1934 [View Article]
     [Google Scholar]
  54. Millán-Aguiñaga N, Chavarria KL, Ugalde JA, Letzel A-C, Rouse GW et al. Phylogenomic insight into Salinispora (bacteria, actinobacteria) species designations. Sci Rep 2017; 7:3564 [View Article]
     [Google Scholar]
  55. Beye M, Fahsi N, Raoult D, Fournier PE. Careful use of 16S rRNA gene sequence similarity values for the identification of Mycobacterium species. New Microbes New Infect 2018; 22:24–29 [View Article]
     [Google Scholar]
  56. Howe JA, Wilson CR, Shimmield TM, Diaz RJ, Carpenter LW. Recent deep-water sedimentation, trace metal and radioisotope geochemistry across the southern ocean and Northern Weddell Sea, Antarctica. Deep Sea Research Part II 2007; 54:1652–1681 [View Article]
     [Google Scholar]
  57. Hou Y, Lin S. Distinct Gene Number-Genome Size Relationships for Eukaryotes and Non-Eukaryotes: Gene Content Estimation for Dinoflagellate Genomes. In Redfield RJ. editor PLoS ONE 4 2009 pp e6978–8 [View Article]
     [Google Scholar]
  58. Koester JA, Swalwell JE, von Dassow P, Armbrust EV. Genome size differentiates co-occurring populations of the planktonic diatom Ditylum brightwellii (Bacillariophyta). BMC Evol Biol 2010; 10:1 [View Article]
     [Google Scholar]
  59. Yang JY, Sanchez LM, Rath CM, Liu X, Boudreau PD et al. Molecular networking as a dereplication strategy. J Nat Prod 2013; 76:1686–1699 [View Article]
     [Google Scholar]
  60. Quinn RA, Nothias L-F, Vining O, Meehan M, Esquenazi E et al. Molecular networking as a drug discovery, drug metabolism, and precision medicine strategy. Trends Pharmacol Sci 2017; 38:143–154 [View Article]
     [Google Scholar]
  61. Tian Y, Li YL, Zhao FC. Secondary metabolites from polar organisms. Mar Drugs 2017; 15:28–30 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000845
Loading
Awakening ancient polar Actinobacteria: diversity, evolution and specialized metabolite potential
Microbiology 165, 1169 (2019); https://doi.org/10.1099/mic.0.000845
/content/journal/micro/10.1099/mic.0.000845
/content/journal/micro/10.1099/mic.0.000845
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error