Longitudinal analysis of the lung microbiota of cynomolgous macaques during long-term SHIV infection

Alison Morris, Joseph N. Paulson, Hisham Talukder, Laura Tipton, Heather Kling, Lijia Cui, Adam Fitch, Mihai Pop, Karen A. Norris, Elodie Ghedin

Research output: Contribution to journalArticle

Abstract

Background: Longitudinal studies of the lung microbiome are challenging due to the invasive nature of sample collection. In addition, studies of the lung microbiome in human disease are usually performed after disease onset, limiting the ability to determine early events in the lung. We used a non-human primate model to assess lung microbiome alterations over time in response to an HIV-like immunosuppression and determined impact of the lung microbiome on development of obstructive lung disease. Cynomolgous macaques were infected with the SIV-HIV chimeric virus SHIV89.6P. Bronchoalveolar lavage fluid samples were collected pre-infection and every 4 weeks for 53 weeks post-infection. The microbiota was characterized at each time point by 16S ribosomal RNA (rRNA) sequencing. Results: We observed individual variation in the composition of the lung microbiota with a proportion of the macaques having Tropheryma whipplei as the dominant organism in their lungs. Bacterial communities varied over time both within and between animals, but there did not appear to be a systematic alteration due to SHIV infection. Development of obstructive lung disease in the SHIV-infected animals was characterized by a relative increase in abundance of oral anaerobes. Network analysis further identified a difference in community composition that accompanied the development of obstructive disease with negative correlations between members of the obstructed and non-obstructed groups. This emphasizes how species shifts can impact multiple other species, potentially resulting in disease. Conclusions: This study is the first to investigate the dynamics of the lung microbiota over time and in response to immunosuppression in a non-human primate model. The persistence of oral bacteria in the lung and their association with obstruction suggest a potential role in pathogenesis. The lung microbiome in the non-human primate is a valuable tool for examining the impact of the lung microbiome in human health and disease.

Original languageEnglish (US)
Article number38
JournalMicrobiome
Volume4
DOIs
StatePublished - 2016

Fingerprint

Microbiota
Macaca
Lung
Infection
Primates
Obstructive Lung Diseases
Immunosuppression
Tropheryma
HIV
Bronchoalveolar Lavage Fluid
Longitudinal Studies
Viruses
Bacteria

Keywords

  • 16S rRNA
  • Microbiota
  • SHIV
  • Time series

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

Cite this

Longitudinal analysis of the lung microbiota of cynomolgous macaques during long-term SHIV infection. / Morris, Alison; Paulson, Joseph N.; Talukder, Hisham; Tipton, Laura; Kling, Heather; Cui, Lijia; Fitch, Adam; Pop, Mihai; Norris, Karen A.; Ghedin, Elodie.

In: Microbiome, Vol. 4, 38, 2016.

Research output: Contribution to journalArticle

Morris, A, Paulson, JN, Talukder, H, Tipton, L, Kling, H, Cui, L, Fitch, A, Pop, M, Norris, KA & Ghedin, E 2016, 'Longitudinal analysis of the lung microbiota of cynomolgous macaques during long-term SHIV infection', Microbiome, vol. 4, 38. https://doi.org/10.1186/s40168-016-0183-0
Morris, Alison ; Paulson, Joseph N. ; Talukder, Hisham ; Tipton, Laura ; Kling, Heather ; Cui, Lijia ; Fitch, Adam ; Pop, Mihai ; Norris, Karen A. ; Ghedin, Elodie. / Longitudinal analysis of the lung microbiota of cynomolgous macaques during long-term SHIV infection. In: Microbiome. 2016 ; Vol. 4.
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abstract = "Background: Longitudinal studies of the lung microbiome are challenging due to the invasive nature of sample collection. In addition, studies of the lung microbiome in human disease are usually performed after disease onset, limiting the ability to determine early events in the lung. We used a non-human primate model to assess lung microbiome alterations over time in response to an HIV-like immunosuppression and determined impact of the lung microbiome on development of obstructive lung disease. Cynomolgous macaques were infected with the SIV-HIV chimeric virus SHIV89.6P. Bronchoalveolar lavage fluid samples were collected pre-infection and every 4 weeks for 53 weeks post-infection. The microbiota was characterized at each time point by 16S ribosomal RNA (rRNA) sequencing. Results: We observed individual variation in the composition of the lung microbiota with a proportion of the macaques having Tropheryma whipplei as the dominant organism in their lungs. Bacterial communities varied over time both within and between animals, but there did not appear to be a systematic alteration due to SHIV infection. Development of obstructive lung disease in the SHIV-infected animals was characterized by a relative increase in abundance of oral anaerobes. Network analysis further identified a difference in community composition that accompanied the development of obstructive disease with negative correlations between members of the obstructed and non-obstructed groups. This emphasizes how species shifts can impact multiple other species, potentially resulting in disease. Conclusions: This study is the first to investigate the dynamics of the lung microbiota over time and in response to immunosuppression in a non-human primate model. The persistence of oral bacteria in the lung and their association with obstruction suggest a potential role in pathogenesis. The lung microbiome in the non-human primate is a valuable tool for examining the impact of the lung microbiome in human health and disease.",
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AU - Tipton, Laura

AU - Kling, Heather

AU - Cui, Lijia

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AB - Background: Longitudinal studies of the lung microbiome are challenging due to the invasive nature of sample collection. In addition, studies of the lung microbiome in human disease are usually performed after disease onset, limiting the ability to determine early events in the lung. We used a non-human primate model to assess lung microbiome alterations over time in response to an HIV-like immunosuppression and determined impact of the lung microbiome on development of obstructive lung disease. Cynomolgous macaques were infected with the SIV-HIV chimeric virus SHIV89.6P. Bronchoalveolar lavage fluid samples were collected pre-infection and every 4 weeks for 53 weeks post-infection. The microbiota was characterized at each time point by 16S ribosomal RNA (rRNA) sequencing. Results: We observed individual variation in the composition of the lung microbiota with a proportion of the macaques having Tropheryma whipplei as the dominant organism in their lungs. Bacterial communities varied over time both within and between animals, but there did not appear to be a systematic alteration due to SHIV infection. Development of obstructive lung disease in the SHIV-infected animals was characterized by a relative increase in abundance of oral anaerobes. Network analysis further identified a difference in community composition that accompanied the development of obstructive disease with negative correlations between members of the obstructed and non-obstructed groups. This emphasizes how species shifts can impact multiple other species, potentially resulting in disease. Conclusions: This study is the first to investigate the dynamics of the lung microbiota over time and in response to immunosuppression in a non-human primate model. The persistence of oral bacteria in the lung and their association with obstruction suggest a potential role in pathogenesis. The lung microbiome in the non-human primate is a valuable tool for examining the impact of the lung microbiome in human health and disease.

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