Signatures of disease outcome severity in the intestinal fungal and bacterial microbiome of COVID-19 patients

被引:6
作者
Rizzello, Fernando [1 ,2 ]
Viciani, Elisa [3 ]
Gionchetti, Paolo [1 ,2 ]
Filippone, Eleonora [1 ,2 ]
Imbesi, Veronica [1 ]
Melotti, Laura [1 ,2 ]
Dussias, Nikolas Konstantine [1 ,2 ]
Salice, Marco [1 ]
Santacroce, Barbara [3 ]
Padella, Antonella [3 ]
Velichevskaya, Alena [3 ]
Marcante, Andrea [3 ]
Castagnetti, Andrea [3 ]
机构
[1] Univ Bologna, Azienda Osped Univ Bologna, IBD Unit, IRCCS, Bologna, Italy
[2] Univ Bologna, Dept Med & Surg & Sci, Bologna, Italy
[3] Wellmicro Srl, Bologna, Italy
关键词
human microbiota; COVID-19; SARS-CoV-2; pathogenesis; mycobiota; microbiome; SCFA (short chain fatty acid); GENE;
D O I
10.3389/fcimb.2024.1352202
中图分类号
R392 [医学免疫学]; Q939.91 [免疫学];
学科分类号
100102 ;
摘要
Background COVID-19, whose causative pathogen is the Severe Acute Respiratory Syndrome Coronavirus-2 (SARS-CoV-2), was declared a pandemic in March 2020. The gastrointestinal tract is one of the targets of this virus, and mounting evidence suggests that gastrointestinal symptoms may contribute to disease severity. The gut-lung axis is involved in the immune response to SARS-CoV-2; therefore, we investigated whether COVID-19 patients' bacterial and fungal gut microbiome composition was linked to disease clinical outcome.Methods In May 2020, we collected stool samples and patient records from 24 hospitalized patients with laboratory-confirmed SARS-CoV-2 infection. Fungal and bacterial gut microbiome was characterized by amplicon sequencing on the MiSeq, Illumina's integrated next generation sequencing instrument. A cohort of 201 age- and sex-matched healthy volunteers from the project PRJNA661289 was used as a control group for the bacterial gut microbiota analysis.Results We observed that female COVID-19 patients had a lower gut bacterial microbiota richness than male patients, which was consistent with a different latency in hospital admittance time between the two groups. Both sexes in the COVID-19 patient study group displayed multiple positive associations with opportunistic bacterial pathogens such as Enterococcus, Streptococcus, and Actinomyces. Of note, the Candida genus dominated the gut mycobiota of COVID-19 patients, and adult patients showed a higher intestinal fungal diversity than elderly patients. We found that Saccharomycetales unassigned fungal genera were positively associated with bacterial short-chain fatty acid (SCFA) producers and negatively associated with the proinflammatory genus Bilophila in COVID-19 patients, and we observed that none of the patients who harbored it were admitted to the high-intensity unit.Conclusions COVID-19 was associated with opportunistic bacterial pathogens, and Candida was the dominant fungal taxon in the intestine. Together, we found an association between commensal SCFA-producers and a fungal genus that was present in the intestines of patients who did not experience the most severe outcome of the disease. We believe that this taxon could have played a role in the disease outcome, and that further studies should be conducted to understand the role of fungi in gastrointestinal and health protection.
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共 62 条
[1]  
[Anonymous], 1908, BIOMETRIKA, V6, P1
[2]   A Guide to COVID-19: a global pandemic caused by the novel coronavirus SARS-CoV-2 [J].
Atzrodt, Cassandra L. ;
Maknojia, Insha ;
McCarthy, Robert D. P. ;
Oldfield, Tiara M. ;
Po, Jonathan ;
Ta, Kenny T. L. ;
Stepp, Hannah E. ;
Clements, Thomas P. .
FEBS JOURNAL, 2020, 287 (17) :3633-3650
[3]   Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 [J].
Bolyen, Evan ;
Rideout, Jai Ram ;
Dillon, Matthew R. ;
Bokulich, NicholasA. ;
Abnet, Christian C. ;
Al-Ghalith, Gabriel A. ;
Alexander, Harriet ;
Alm, Eric J. ;
Arumugam, Manimozhiyan ;
Asnicar, Francesco ;
Bai, Yang ;
Bisanz, Jordan E. ;
Bittinger, Kyle ;
Brejnrod, Asker ;
Brislawn, Colin J. ;
Brown, C. Titus ;
Callahan, Benjamin J. ;
Caraballo-Rodriguez, Andres Mauricio ;
Chase, John ;
Cope, Emily K. ;
Da Silva, Ricardo ;
Diener, Christian ;
Dorrestein, Pieter C. ;
Douglas, Gavin M. ;
Durall, Daniel M. ;
Duvallet, Claire ;
Edwardson, Christian F. ;
Ernst, Madeleine ;
Estaki, Mehrbod ;
Fouquier, Jennifer ;
Gauglitz, Julia M. ;
Gibbons, Sean M. ;
Gibson, Deanna L. ;
Gonzalez, Antonio ;
Gorlick, Kestrel ;
Guo, Jiarong ;
Hillmann, Benjamin ;
Holmes, Susan ;
Holste, Hannes ;
Huttenhower, Curtis ;
Huttley, Gavin A. ;
Janssen, Stefan ;
Jarmusch, Alan K. ;
Jiang, Lingjing ;
Kaehler, Benjamin D. ;
Bin Kang, Kyo ;
Keefe, Christopher R. ;
Keim, Paul ;
Kelley, Scott T. ;
Knights, Dan .
NATURE BIOTECHNOLOGY, 2019, 37 (08) :852-857
[4]  
Callahan Ben J, 2016, F1000Res, V5, P1492
[5]  
Callahan BJ, 2016, NAT METHODS, V13, P581, DOI [10.1038/nmeth.3869, 10.1038/NMETH.3869]
[6]   Clostridium innocuum is a significant vancomycin-resistant pathogen for extraintestinal clostridial infection [J].
Chia, J. -H. ;
Feng, Y. ;
Su, L. -H. ;
Wu, T. -L. ;
Chen, C. -L. ;
Liang, Y. -H. ;
Chiu, C. -H. .
CLINICAL MICROBIOLOGY AND INFECTION, 2017, 23 (08) :560-566
[7]   Mechanisms Leading to Gut Dysbiosis in COVID-19: Current Evidence and Uncertainties Based on Adverse Outcome Pathways [J].
Clerbaux, Laure-Alix ;
Fillipovska, Julija ;
Munoz, Amalia ;
Petrillo, Mauro ;
Coecke, Sandra ;
Amorim, Maria-Joao ;
Grenga, Lucia .
JOURNAL OF CLINICAL MEDICINE, 2022, 11 (18)
[8]   Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data [J].
Davis, Nicole M. ;
Proctor, Diana M. ;
Holmes, Susan P. ;
Relman, David A. ;
Callahan, Benjamin J. .
MICROBIOME, 2018, 6
[9]   Role of the Microbiome in the Pathogenesis of COVID-19 [J].
De, Rituparna ;
Dutta, Shanta .
FRONTIERS IN CELLULAR AND INFECTION MICROBIOLOGY, 2022, 12
[10]   The Gut-Lung Axis in Health and Respiratory Diseases: A Place for Inter-Organ and Inter-Kingdom Crosstalks [J].
Enaud, Raphael ;
Prevel, Renaud ;
Ciarlo, Eleonora ;
Beaufils, Fabien ;
Wieers, Gregoire ;
Guery, Benoit ;
Delhaes, Laurence .
FRONTIERS IN CELLULAR AND INFECTION MICROBIOLOGY, 2020, 10