Characterisation ofOrnithobacterium hominiscolonisation dynamics and interaction with the nasopharyngeal microbiome in a South African birth cohort

  1. Celine C De Allende
  2. Susannah J Salter
  3. Siobhan E Brigg
  4. Shantelle Claassen-Weitz
  5. Kilaza S Mwaikono
  6. Lesley Workman
  7. Heather J Zar
  8. Mark P Nicol
  9. Julian Parkhill
  10. Felix S Dube
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Abstract

Ornithobacterium hominisis a recently described Gram-negative bacterium that colonises the human nasopharynx and may be associated with poor upper respiratory tract health. Here, we describe the isolation ofO. hominisfrom samples collected from a South African birth cohort, creating the first archive of cultured strains of the species from Africa. Sequenced genomes from this archive reveal that South AfricanO. hominisis more similar to Australian strains than those from Southeast Asia, and that it may share genes with other members of the microbiome that are relevant for virulence, colonisation, and antibiotic resistance. Leveraging existing microbiome data from the cohort,O. hominiswas found to be closely associated with bacterial co-colonisers that are rare in non-carrier individuals, includingSuttonella,Helcococcus,Moraxellaspp., and Gracilibacteria. Their collective acquisition has a significant impact on the diversity of nasopharyngeal communities that containO. hominis. Individuals who have not yet acquiredO. hominishave a higher abundance ofMoraxella(particularlyM. lincolnii) than individuals who never acquireO. hominis, suggesting that this could be a precursor state for successful colonisation. Finally, a novel co-coloniser species,Helcococcus ekapensis, was successfully isolated and sequenced.

Data Summary

Ornithobacterium hominisdata have been deposited under project accession ERP149886. This comprises genome sequences for isolates SA-OH-C1 (ERR13967269), SA-OH-C2 (ERR13967270), SA-OH-C3 (ERR13967271), SA-OH-C4 (ERR13967272, ERR13967275), SA-OH-C5 (ERR13967273), SA-OH-C6 (ERR13967274, ERR13967276). Previously published 16S rRNA gene data are deposited under project accessions PRJNA790843 and PRJNA548658.Helcococcus ekapensisgenome data are deposited under project accession PRJEB85661.

Software used

  • AMRFinderPlus v3.12.8:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/ncbi/amr">https://github.com/ncbi/amr</ext-link>

  • AssembleBAC-ONT v1.1.1:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/avantonder/assembleBAC-ONT">https://github.com/avantonder/assembleBAC-ONT</ext-link>

  • BAKTA v1.8.1:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://bakta.computational.bio/">https://bakta.computational.bio/</ext-link>

  • BLAST v2.16.0:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://blast.ncbi.nlm.nih.gov/Blast.cgi">https://blast.ncbi.nlm.nih.gov/Blast.cgi</ext-link>

  • Comprehensive Antibiotic Resistance Database (CARD) Resistance Gene Identifier (RGI) tool v1.2.1:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://card.mcmaster.ca/analyze/rgi">https://card.mcmaster.ca/analyze/rgi</ext-link>

  • Decontam v1.12 (R package):<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/benjjneb/decontam">https://github.com/benjjneb/decontam</ext-link>

  • Eggnog-mapper v2.0.1:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://eggnog-mapper.embl.de/">http://eggnog-mapper.embl.de/</ext-link>

  • FastANI v1.1.0:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/ParBLiSS/FastANI">https://github.com/ParBLiSS/FastANI</ext-link>

  • Flye v2.9.2:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/fenderglass/Flye">https://github.com/fenderglass/Flye</ext-link>

  • Guppy v6.5.7:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://community.nanoporetech.com/downloads/guppy/release_notes">https://community.nanoporetech.com/downloads/guppy/release_notes</ext-link>

  • ISEScan v1.7.2.3:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://usegalaxy.eu/root?tool_id=toolshed.g2.bx.psu.edu/repos/iuc/isescan/isescan/1.7.2.3+galaxy1">https://usegalaxy.eu/root?tool_id=toolshed.g2.bx.psu.edu/repos/iuc/isescan/isescan/1.7.2.3+galaxy1</ext-link>

  • Medaka v1.9.1:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/nanoporetech/medaka">https://github.com/nanoporetech/medaka</ext-link>

  • MEGA11:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://www.megasoftware.net/">https://www.megasoftware.net/</ext-link>

  • MMseqs2 v17:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/soedinglab/MMseqs2">https://github.com/soedinglab/MMseqs2</ext-link>

  • Mothur v1.44.3:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/mothur/mothur">https://github.com/mothur/mothur</ext-link>

  • NetCoMi v1.2.0 (R package):<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/stefpeschel/NetCoMi">https://github.com/stefpeschel/NetCoMi</ext-link>

  • Panaroo v1.4.3:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/gtonkinhill/panaroo">https://github.com/gtonkinhill/panaroo</ext-link>

  • PHASTEST:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://phastest.ca/submissions/new">https://phastest.ca/submissions/new</ext-link>

  • Prowler (commit ID c3041ba):<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://github.com/ProwlerForNanopore/ProwlerTrimmer">https://github.com/ProwlerForNanopore/ProwlerTrimmer</ext-link>

  • R v4.4.3:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://www.r-project.org/">https://www.r-project.org/</ext-link>

Databases used

  • Comprehensive Antibiotic Resistance Database (CARD):<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://card.mcmaster.ca/">https://card.mcmaster.ca/</ext-link>

  • European Nucleotide Archive:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://www.ebi.ac.uk/ena/">https://www.ebi.ac.uk/ena/</ext-link>

  • Genome Taxonomy Database (GTDB) release 09-RS220:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://gtdb.ecogenomic.org/">https://gtdb.ecogenomic.org/</ext-link>

  • RefSeq release 228:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://www.ncbi.nlm.nih.gov/refseq/about/prokaryotes/">https://www.ncbi.nlm.nih.gov/refseq/about/prokaryotes/</ext-link>

  • SILVA v132:<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="https://www.arb-silva.de/">https://www.arb-silva.de/</ext-link>

Impact statement

First described in 2019,Ornithobacterium hominisis an understudied bacterium that may be associated with poor respiratory health in children. The study builds upon existing knowledge ofO. hominisby describing the first African isolates of the species, its potential as a reservoir of virulence and antibiotic resistance genes in the upper respiratory tract, and the unique microbiome profile ofO. hominiscarriers.

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