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Antibiotics-Induced Monodominance of a Novel Gut Bacterial Order

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Antibiotics-Induced Monodominance of a Novel Gut Bacterial Order Gut microbiota ORIGINAL ARTICLE Antibiotics-induced monodominance of a novel gut Gut: first published as 10.1136/gutjnl-2018-317715 on 18 January 2019. Downloaded from bacterial order Falk Hildebrand,1 Lucas Moitinho-Silva,1 Sonja Blasche,1 Martin T Jahn,2 Toni Ingolf Gossmann,3 Jaime Huerta-Cepas,1,4 Rajna Hercog,5 Mechthild Luetge,1 Mohammad Bahram,6,7 Anna Pryszlak,1 Renato J Alves,1,8 Sebastian M Waszak,9 Ana Zhu,1,10 Lumeng Ye,11 Paul Igor Costea,1 Steven Aalvink,12 Clara Belzer,12 Sofia K Forslund,1,13 Shinichi Sunagawa,1,14 Ute Hentschel,2 Christoph Merten,1 Kiran Raosaheb Patil,1 Vladimir Benes,1 Peer Bork1,15,16 ► Additional material is ABSTRact published online only. To view Objective The composition of the healthy human Significance of the study please visit the journal online adult gut microbiome is relatively stable over prolonged (http:// dx. doi. org/ 10. 1136/ What is already known on the subject? gutjnl- 2018- 317715). periods, and representatives of the most highly abundant and prevalent species have been cultured and ► Antibiotic treatments are known to reduce For numbered affiliations see bacterial diversity short term, recovering usually end of article. described. However, microbial abundances can change on perturbations, such as antibiotics intake, enabling within weeks. ► Antibiotic-associated diarrhoea can be Correspondence to the identification and characterisation of otherwise low Professor Peer Bork, Structural abundant species. associated to blooms of pathogenic bacteria, and Computational Biology Design Analysing gut microbial time-series data, like Clostridium difficile, although the cause is Unit, European Molecular we used shotgun metagenomics to create strain level often also unknown. Biology Laboratory, Heidelberg ► Most abundant bacteria of the human gut 69117, Germany; bork@ embl. de taxonomic and functional profiles.C ommunity dynamics were modelled postintervention with a focus on microbiome are characterised and sequenced, Received 8 October 2018 conditionally rare taxa and previously unknown bacteria. but much less is known about the rare Revised 17 December 2018 Results In response to a commonly prescribed biosphere. Accepted 19 December 2018 cephalosporin (ceftriaxone), we observe a strong compositional shift in one subject, in which a previously U What are the new findings? unknown species, Borkfalki ceftriaxensis, was identified, ► A member of an undiscovered order of http://gut.bmj.com/ blooming to 92% relative abundance. The genome Firmicutes that is prevalent in one-third of assembly reveals that this species (1) belongs to a so human gut samples, bloomed in multiple far undescribed order of Firmicutes, (2) is ubiquitously individuals after treatment with antibiotics. present at low abundances in at least one third of adults, During blooming, it rose to 92% relative (3) is opportunistically growing, being ecologically similar abundance, corresponding to a 2000-fold to typical probiotic species and (4) is stably associated increase in absolute abundance. on October 1, 2021 by guest. Protected copyright. to healthy hosts as determined by single nucleotide ► The extreme bloom uncovers for the first-time variation analysis. It was the first coloniser after the monodominant states in the adult gut by antibiotic intervention that led to a long-lasting microbial commensal bacteria. This was further reinforced community shift and likely permanent loss of nine by a second commensal, Parabacteroides commensals. U distasonis, also becoming monodominant at Conclusion The bloom of B. ceftriaxensis and 95% relative abundance. a subsequent one of Parabacteroides distasonis ► Nine commensal bacteria are absent in all time demonstrate the existence of monodominance points after the extreme community reshaping, community states in the gut. Our study points to an further confirmed using complete genome undiscovered wealth of low abundant but common mappings. taxa in the human gut and calls for more highly ► A recurrent bacterial network response is resolved longitudinal studies, in particular on ecosystem observed after cephalosporin antibiotic perturbations. treatment. © Author(s) (or their employer(s)) 2019. Re-use permitted under CC BY. How might it impact on clinical practice in the Published by BMJ. INTRODUCTION foreseeable future? The gut microbiota plays an important role in ► This study highlights the detrimental impact of To cite: Hildebrand F, human health1 2 and is characterised by a diverse Moitinho-Silva L, Blasche S, antibiotics on the adult gut microbiome, as well et al. Gut Epub ahead of community and complex genetic variation land- as shedding light on the recolonisation process, print: [please include Day scape deducible from shotgun metagenomics leading to ecosystem insights into antibiotic 3 Month Year]. doi:10.1136/ data. Compared with the skin or oral cavity, GI side effects. gutjnl-2018-317715 microbiomes are remarkably stable over prolonged Hildebrand F, et al. Gut 2019;0:1–10. doi:10.1136/gutjnl-2018-317715 1 Gut microbiota periods,4 which in particular applies to the more highly abun- we performed de novo assembly of HD.S1.374 and metage- dant species.5 Much less attention has, however, been paid to nomic gene-level analysis, which both showed a single, hitherto low abundant species, despite having important keystone func- unknown species, dominating this sample at 92% relative abun- Gut: first published as 10.1136/gutjnl-2018-317715 on 18 January 2019. Downloaded from tions in the human gut6 and explaining most of the temporal dance (online supplementary figure 1). Attempts to culture this variation through conditionally rare taxa (CRT).7 The abun- species were not successful (see online supplementary tables 1 dance range is usually limited and extreme relative abundances and 2), but we were able to assemble the species’ genome with exceeding 60% are only defined for forest ecosystems as mono- a quality comparable to assemblies from cultured species (see dominance.8 Nonetheless, monodominance can be observed, for online supplementary tables 3 and 4). The conserved 16S rRNA example, during the first days after birth in human gut micro- gene sequence was very divergent (≤86% nucleotide (nt) iden- biomes9 or in adults during infectious diarrhoea (typically asso- tity) to known bacteria (see the UB. ceftriaxensis belongs to a new ciated to Proteobacteria such as Vibrio cholera or Escherichia order of Firmicutes section). Since the genome assembly is based coli10). Frequently, however, the infectious source of diarrhoea solely on metagenomics, we named it UB. ceftriaxensis gen. nov., remains unidentified,11 and little is known of the role of CRTs in sp. nov., following the nomenclature proposed for uncultured the recolonisation of the gut microbiome after exogenous distur- species.17 bances, such as antibiotic treatments. Using fluorescence in situ hybridisation (FISH) (see online This knowledge gap is compounded by CRTs often not supplementary file 1), we could detect UB. ceftriaxensis in being represented in genome collections12 or ill-defined. CRTs faecal samples (figure 1D), demonstrating that it was present in are often not detectable in metagenomes, because they are per the stool. Labelled cells were rod shaped and on average 1.5 definition rare and therefore difficult to spot with standard (±0.3)×0.8 (± 0.1) μm long and wide (online supplementary metagenomic approaches that rely on having either a reference table 5). Functional analysis of its gene content indicated that genome in databases13 14 or sufficient read coverage in multiple it is a facultative anaerobe spore-forming fermenter, with a samples to de novo construct metagenomic assembled genomes large spectrum of monosaccharide and oligosaccharide utilisa- (MAGs).15 But even with reconstructed MAGs, insights on the tion genes (figure 1C, online supplementary figure 2 and table ecological role of these novel species remain usually limited as 6 for a complete description). Its predicted fermentation prod- the functional annotation of MAGs is often automatic. ucts include two of the three short-chain fatty acids, acetate and To investigate microbial dynamics in response to antibi- propionate. otic perturbations and the influence of CRTs, we leveraged an The discovery of UB. ceftriaxensis was enabled by its bloom extensive longitudinal sampling and respective metagenome after beta-lactam ceftriaxone treatment. We identified two genes sequencing16 (see online supplementary file 1). We found that distantly related to beta-lactamases, but in vitro tests showed a novel bacterial species, UBorkfalki ceftriaxensis, which belongs only modest activity (see online supplementary file 1). Instead, to a new order of Firmicutes and bloomed during the first 3 days it seems most likely that UB. ceftriaxensis is inherently resilient after antibiotic treatment to monodominant levels. UB. ceftriax- to ceftriaxone, due to its penicillin binding proteins of classes ensis is thus the first report of a gut conditionally monodominant known to confer resistance in gram positive bacteria (see online taxa (CMT) that is not invasive. Instead, it is globally prevalent supplement discussion) and due to its spore-forming ability.18 Its in the population, but only associated to humans in our anal- predicted diversified carbohydrate metabolism makes it plausible ysis of >3500 metagenomic samples. The initial colonisation by that UB. ceftriaxensis can grow extremely fast in an ecosystem http://gut.bmj.com/ this species was succeeded by a second
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