Women with type 1 diabetes exhibit a progressive increase in gut Saccharomyces cerevisiae in pregnancy associated with evidence of gut inflammation

Esther Bandala-Sanchez; Alexandra J Roth-Schulze; Helena Oakey; Megan A S Penno; Naiara G Bediaga; Gaetano Naselli; Katrina M Ngui; Alannah D Smith; Dexing Huang; Enrique Zozaya-Valdes; Rebecca L Thomson; James D Brown; Peter J Vuillermin; Simon C Barry; Maria E Craig; William D Rawlinson; Elizabeth A Davis; Mark Harris; Georgia Soldatos; Peter G Colman; John M Wentworth; Aveni Haynes; Grant Morahan; Richard O Sinnott; Anthony T Papenfuss; Jennifer J Couper; Leonard C Harrison; ENDIA Study Group

doi:10.1016/j.diabres.2022.109189

Women with type 1 diabetes exhibit a progressive increase in gut Saccharomyces cerevisiae in pregnancy associated with evidence of gut inflammation

Diabetes Res Clin Pract. 2022 Feb:184:109189. doi: 10.1016/j.diabres.2022.109189. Epub 2022 Jan 18.

Authors

Esther Bandala-Sanchez¹, Alexandra J Roth-Schulze¹, Helena Oakey², Megan A S Penno², Naiara G Bediaga¹, Gaetano Naselli¹, Katrina M Ngui¹, Alannah D Smith¹, Dexing Huang¹, Enrique Zozaya-Valdes¹, Rebecca L Thomson², James D Brown², Peter J Vuillermin³, Simon C Barry², Maria E Craig⁴, William D Rawlinson⁵, Elizabeth A Davis⁶, Mark Harris⁷, Georgia Soldatos⁸, Peter G Colman⁹, John M Wentworth¹⁰, Aveni Haynes⁶, Grant Morahan¹¹, Richard O Sinnott¹², Anthony T Papenfuss¹³, Jennifer J Couper¹⁴, Leonard C Harrison¹⁵; ENDIA Study Group

Affiliations

¹ Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia; Department of Medical Biology, University of Melbourne, Melbourne, VIC, Australia.
² The University of Adelaide, Robinson Research Institute, Adelaide Medical School, University of Adelaide, Adelaide, SA, Australia.
³ Faculty of School of Medicine, Deakin University and Child Health Research Unit, Barwon Health, Geelong, VIC, Australia.
⁴ School of Women's and Children's Health, Faculty of Medicine, University of New South Wales, Sydney, NSW, Australia; Institute of Endocrinology and Diabetes, The Children's Hospital at Westmead, Sydney, NSW, Australia.
⁵ Virology Research Laboratory, Serology and Virology Division, South Eastern Area Laboratory Services Microbiology, NSW Health Pathology, Sydney, NSW, Australia; School of Medical Sciences, Biotechnology and Biomolecular Sciences, Women's and Children's Health, University of New South Wales, Sydney, NSW, Australia.
⁶ Telethon Institute for Child Health Research, Centre for Child Health Research, University of Western Australia, Perth, WA, Australia.
⁷ The University of Queensland Diamantina Institute, Faculty of Medicine, University of Queensland, Translational Research Institute, Woolloongabba, QLD, Australia; Queensland Children's Hospital, South Brisbane, QLD, Australia.
⁸ Monash Centre for Health Research and Implementation, School of Public Health and Preventive Medicine, Monash University, Melbourne and Diabetes and Vascular Medicine Unit, Monash Health, Melbourne, VIC, Australia.
⁹ Department of Diabetes and Endocrinology, Royal Melbourne Hospital, Melbourne, VIC, Australia.
¹⁰ Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia; Department of Medical Biology, University of Melbourne, Melbourne, VIC, Australia; Department of Diabetes and Endocrinology, Royal Melbourne Hospital, Melbourne, VIC, Australia.
¹¹ Centre for Diabetes Research, Harry Perkins Institute of Medical Research, The University of Western Australia, Perth, WA, Australia.
¹² Melbourne eResearch Group, School of Computing and Information Services, University of Melbourne, Melbourne, VIC, Australia.
¹³ Walter and Eliza Hall Institute of Medical Research, Melbourne, VIC, Australia; Department of Medical Biology and School of Mathematics and Statistics, University of Melbourne, Melbourne, VIC, Australia; Bioinformatics and Cancer Genomics Laboratory, Peter MacCallum Cancer Centre, Melbourne, VIC, Australia; Sir Peter MacCallum Department of Oncology, University of Melbourne, Parkville, VIC, Australia.
¹⁴ The University of Adelaide, Robinson Research Institute, Adelaide Medical School, University of Adelaide, Adelaide, SA, Australia; Women's and Children's Hospital, Adelaide, SA, Australia.
¹⁵ Walter and Eliza Hall Institute of Medical Research, Melbourne, Australia; Department of Medical Biology, University of Melbourne, Melbourne, VIC, Australia. Electronic address: harrison@wehi.edu.au.

PMID: 35051423
DOI: 10.1016/j.diabres.2022.109189

Abstract

Aims: Studies of the gut microbiome have focused on its bacterial composition. We aimed to characterize the gut fungal microbiome (mycobiome) across pregnancy in women with and without type 1 diabetes.

Methods: Faecal samples (n = 162) were collected from 70 pregnant women (45 with and 25 without type 1 diabetes) across all trimesters. Fungi were analysed by internal transcribed spacer 1 amplicon sequencing. Markers of intestinal inflammation (faecal calprotectin) and intestinal epithelial integrity (serum intestinal fatty acid binding protein; I-FABP), and serum antibodies to Saccharomyces cerevisiae (ASCA) were measured.

Results: Women with type 1 diabetes had decreased fungal alpha diversity by the third trimester, associated with an increased abundance of Saccharomyces cerevisiae that was inversely related to the abundance of the anti-inflammatory butyrate-producing bacterium Faecalibacterium prausnitzii. Women with type 1 diabetes had higher concentrations of calprotectin, I-FABP and ASCA.

Conclusions: Women with type 1 diabetes exhibit a shift in the gut mycobiome across pregnancy associated with evidence of gut inflammation and impaired intestinal barrier function. The relevance of these findings to the higher rate of pregnancy complications in type 1 diabetes warrants further study.

Keywords: Faecalibacterium prausnitzii; Fungi; Gut; ITS1; Inflammation; Microbiome; Mycobiome; Pregnancy; Saccharomyces; Type 1 diabetes.

MeSH terms

Diabetes Mellitus, Type 1*
Feces / microbiology
Female
Gastrointestinal Microbiome* / genetics
Humans
Inflammation
Mycobiome*
Pregnancy
Saccharomyces cerevisiae