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Journal.Pone.0146926 King’s Research Portal DOI: 10.1371/journal.pone.0146926 Document Version Publisher's PDF, also known as Version of record Link to publication record in King's Research Portal Citation for published version (APA): Vartoukian, S. R., Adamowska, A., Lawlor, M., Moazzez, R., Dewhirst, F. E., & Wade, W. G. (2016). In Vitro Cultivation of ‘Unculturable’ Oral Bacteria, Facilitated by Community Culture and Media Supplementation with Siderophores. PLOS One. https://doi.org/10.1371/journal.pone.0146926 Citing this paper Please note that where the full-text provided on King's Research Portal is the Author Accepted Manuscript or Post-Print version this may differ from the final Published version. If citing, it is advised that you check and use the publisher's definitive version for pagination, volume/issue, and date of publication details. 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Download date: 04. Oct. 2021 RESEARCH ARTICLE In Vitro Cultivation of ‘Unculturable’ Oral Bacteria, Facilitated by Community Culture and Media Supplementation with Siderophores Sonia R. Vartoukian1, Aleksandra Adamowska1, Megan Lawlor1, Rebecca Moazzez2, Floyd E. Dewhirst3,4, William G. Wade1* 1 Barts and The London School of Medicine and Dentistry, Queen Mary University of London, London, United Kingdom, 2 King’s College London Dental Institute, London, United Kingdom, 3 The Forsyth Institute, Cambridge, United States of America, 4 Harvard School of Dental Medicine, Boston, United States of America * [email protected] Abstract OPEN ACCESS Over a third of oral bacteria are as-yet-uncultivated in-vitro. Siderophores have been previ- Citation: Vartoukian SR, Adamowska A, Lawlor M, ously shown to enable in-vitro growth of previously uncultivated bacteria. The objective of Moazzez R, Dewhirst FE, Wade WG (2016) In Vitro this study was to cultivate novel oral bacteria in siderophore-supplemented culture media. Cultivation of ‘Unculturable’ Oral Bacteria, Facilitated by Various compounds with siderophore activity, including pyoverdines-Fe-complex, desferri- Community Culture and Media Supplementation with Siderophores. PLoS ONE 11(1): e0146926. coprogen and salicylic acid, were found to stimulate the growth of difficult-to-culture strains doi:10.1371/journal.pone.0146926 Prevotella sp. HOT-376 and Fretibacterium fastidiosum. Furthermore, pyrosequencing Editor: Zezhang Wen, LSU Health Sciences Center analysis demonstrated increased proportions of the as-yet-uncultivated phylotypes Dialister School of Dentistry, UNITED STATES sp. HOT-119 and Megasphaera sp. HOT-123 on mixed culture plates supplemented with μ Received: November 12, 2015 siderophores. Therefore a culture model was developed, which incorporated 15 g sidero- phore (pyoverdines-Fe-complex or desferricoprogen) or 150 μl neat subgingival-plaque Accepted: December 23, 2015 suspension into a central well on agar plates that were inoculated with heavily-diluted sub- Published: January 14, 2016 gingival-plaque samples from subjects with periodontitis. Colonies showing satellitism were Copyright: © 2016 Vartoukian et al. This is an open passaged onto fresh plates in co-culture with selected helper strains. Five novel strains, rep- access article distributed under the terms of the resentatives of three previously-uncultivated taxa (Anaerolineae bacterium HOT-439, the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any first oral taxon from the Chloroflexi phylum to have been cultivated; Bacteroidetes bacterium medium, provided the original author and source are HOT-365; and Peptostreptococcaceae bacterium HOT-091) were successfully isolated. All credited.. novel isolates required helper strains for growth, implying dependence on a biofilm lifestyle. Data Availability Statement: Partial 16S rRNA gene Their characterisation will further our understanding of the human oral microbiome. sequences for the novel taxa detected in this study have been submitted to the DDBJ/EMBL/GenBank databases under the following accession numbers: Bacteroidetes bacterium HOT-365 SP18_29, KT861603; Chloroflexi taxon Anaerolineae bacterium Introduction HOT-439 SP9_5, KT861598; Chloroflexi taxon Anaerolineae bacterium HOT-439 SP10_2, The human oral microbiome is composed of a diverse community of bacteria, fungi, protozoa, KT861597; Chloroflexi taxon Anaerolineae bacterium viruses and archaea [1]. When the symbiotic relationship between the oral microbiota and host HOT-439 SP19_9, KT861599. breaks down, a dysbiotic microbial community is established, a change associated with two of Funding: Research reported in this publication was the commonest bacterial diseases of man: periodontitis (gum disease) and dental caries (tooth supported by The National Institute of Dental and decay) [2]. Recent evidence indicates that oral bacteria also have a significant impact on PLOS ONE | DOI:10.1371/journal.pone.0146926 January 14, 2016 1/19 Culture of Previously Uncultured Oral Bacteria Craniofacial Research of the National Institutes of systemic health and disease. For example, it has been shown that oral bacteria are involved in Health under awards R37DE016937 and reduction of dietary nitrate and consequent release of nitric oxide systemically, with a resultant R01DE024468. The funders had no role in study blood-pressure lowering effect [3]. design, data collection and analysis, decision to publish, or preparation of the manuscript. The advent of next generation sequencing has led to a better appreciation of the true diver- sity of the human oral bacteriome, and release 13 of the Human Oral Microbiome Database Competing Interests: The authors have declared (HOMD) (www.homd.org) lists approximately 700 taxa at species level. However, over a third that no competing interests exist. of these, nearly 250, are as yet uncultivated and primarily known only by 16S rRNA gene sequence data [4, 5]. Members of the candidate bacterial Divisions SR1 and GN02 have been frequently detected in molecular 16S rDNA analyses of human (oral) and other samples, but none have ever been cultivated in vitro [6]. Based on molecular analyses, representatives of the TM7 phylum have been found in high prevalence in the oral cavity, and yet, until the recent cultivation of strain TM7x [7], there were no cultivated members. Although the phylum Chlor- oflexi includes several cultivable species, no taxon found in the human oral cavity has been suc- cessfully cultivated [6]. An exploration of the possible reasons for bacteria being uncultivable in the laboratory has been reviewed previously [8, 9]. Arguably, the primary reason for the resistance of bacteria to in vitro cultivation (in isolation) is a dependence on other bacteria and on chemical signals within mixed communities. This may be particularly relevant to bacteria inhabiting biofilm- type communities, such as dental plaque, where metabolic cooperation and intercellular signal- ing networks are widespread [10]. Furthermore, the sharing of metabolites, such as iron-chelat- ing siderophores, within bacterial communities is prevalent particularly in bacteria-host environments [11, 12], and it has been suggested that the ability to produce such siderophores may have been lost in certain ‘unculturable’ bacteria [13]. In light of the above, efforts to cultivate ‘unculturable’ bacteria have sometimes focused on using either a ‘simulated natural environment’ [14, 15], adding chemical factors that are thought to be required (but not produced) by difficult-to-grow bacteria to culture media [16, 17], or using co-culture with other bacteria from the same community to facilitate growth of dependent strains [18, 19]. Despite a wealth of information having been gained in recent years through metagenomic, metaproteomic, metatranscriptomic and other ‘meta-omic’ analyses of microbial communities [20], it is only through the isolation and culture of individual species that phenotypic and geno- typic characteristics can be comprehensively characterised, and virulence potential systemati- cally investigated. On the basis that as-yet-uncultivated bacteria are equally likely to play a role in disease processes as are previously-cultivated bacteria, it is clear that the quest to cultivate them is a most important one. The aims of this study were: (a) to investigate various siderophore-like agents for a growth- stimulatory effect on ‘difficult-to-culture’ oral bacteria; and (b) to develop an in-vitro culture model for the cultivation and isolation of previously-uncultivated oral bacteria, using various means, including community culture and provision of siderophores
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