Evaluation of gut bacterial community composition and antimicrobial resistome in pregnant and non-pregnant women from Saudi population

Infection and Drug Resistance Dovepress open access to scientific and medical research Infection and Drug Resistance downloaded from https://www.dovepress.com/ by 88.198.20.149 on 23-Sep-2019 For personal use only. Open Access Full Text Article Evaluation of gut bacterial community composition and antimicrobial resistome in pregnant and non-pregnant women from Saudi population This article was published in the following Dove Press journal: Infection and Drug Resistance Imran Khan 1–3, * Muhammad Yasir 1,4, * Muhammad Farman 1,5 Taha Kumosani 6 Samera F AlBasri 7 Osama S Bajouh 7 Esam I Azhar 1,4 1 Special Infectious Agents Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; 2 Biochemistry Department, Faculty of Science; Special Infectious Agents Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; 3 State Key Laboratory of Quality Research in Chinese Medicine, Macau University of Science and Technology Taipa, Macau, People’s Republic of China; 4Medical Laboratory Technology Department, Faculty of Applied Medical Sciences, King Abdulaziz University, Jeddah, Saudi Arabia; 5 Department of Biology, King Abdulaziz University, Jeddah, Saudi Arabia; 6 Biochemistry Department, Faculty of Science; Production of Bio-products for Industrial Applications Research Group, and Experimental Biochemistry Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia; 7 Department of Obstetrics & Gynecology, King Abdul Aziz University Hospital, Jeddah, Saudi Arabia *These authors contributed equally to this work Background: Gut microbiota (GM) has recently been described as a functional reservoir of antimicrobial resistant genes (ARGs). However, the ARG-carrying bacterial species in the human gut has been poorly studied. This study, for the first time, is reporting bacterial communities' composition and antimicrobial resistome in the stool samples of pregnant and non-pregnant (NP) Saudi females. Methods: Gut bacterial community composition was analyzed by 16S amplicon sequencing and culturomics. High throughput MALDI-TOF technique was used for identification of the isolates from stool samples and evaluated for resistance against 13 antibiotics using the agar dilution method. Clinically important ARGs were PCR amplified from genomic DNA of the stool samples using gene-specific primers. Results: 16S amplicon sequencing revealed that GM of pregnant and NP women were predominantly comprised of phyla Firmicutes, Bacteroidetes, Proteobacteria, and Actinobacteria. Bacterial diversity decreased in pregnant groups, whereas phylum Bacteroidetes declined significantly (p<0.05) in the first trimester. We noticed a relatively high abundance of butyrateproducing bacteria (eg, Faecalibacterium spp. and Eubacterium spp.) in the gut of pregnant women, whereas Prevotella copri was found at significantly (p<0.01) higher abundance in NP women. Moreover, about 14,694 isolates were identified and classified into 132 distinct species. The majority of the species belonged to phyla Firmicutes and Proteobacteria. About 8,125 isolates exhibited resistance against antibiotics. Out of 73 resistant-species, Enterococcus was the most diverse genus and Escherichia coli was the highly prevalent bacterium. The majority of the isolates were resistant to antibiotics; trimethoprim/sulfamethoxazole, cycloserine, and cefixime. ARGs encoding resistance against aminoglycoside, macrolide, quinolone, β-lactam, and tetracycline antibiotics were predominantly found in genomic DNA of the stool samples. Conclusion: We conclude that pregnancy-associated GM modulations may help to sustain a healthy pregnancy, but a higher proportion of antibiotic resistance could be deleterious for both maternal and fetal health. Keywords: gut microbiota, antimicrobial resistance, metagenomics, culturomics, pregnancy, Saudi Arabia Correspondence: Muhammad Yasir Special Infectious Agents Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah 21589, Saudi Arabia Tel +96 656 320 2241 Email Introduction submit your manuscript | www.dovepress.com Infection and Drug Resistance 2019:12 1749–1761 DovePress © 2019 Khan et al. This work is published and licensed by Dove Medical Press Limited. The full terms of this license are available at https://www.dovepress.com/terms.php and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (http://creativecommons.org/licenses/by-nc/3.0/). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed. For permission for commercial use of this work, please see paragraphs 4.2 and 5 of our Terms (https://www.dovepress.com/terms.php). http://doi.org/10.2147/IDR.S200213 Powered by TCPDF (www.tcpdf.org) ORIGINAL RESEARCH During pregnancy, women undergo complex physiological changes that are accompanied by changes in the diversity and composition of gut microbiota (GM).1,2 Any change in GM composition and diversity may eventually affect host immunity, 1749 Dovepress Infection and Drug Resistance downloaded from https://www.dovepress.com/ by 88.198.20.149 on 23-Sep-2019 For personal use only. Khan et al digestion, and metabolism.3–5 Pregnancy-associated GM modulations, especially an enriched abundance of the phyla Proteobacteria and Actinobacteria, have been associated with the increased energy uptake that occurs during pregnancy.2,6 The health implications of pregnancy-associated GM modulation are still unclear; first, because GM diversity and composition are plastic in nature and vary significantly with geography and diet,7 and secondly, because the pregnancy–GM association has been studied in only a few geographical locations.1,2,8–10 In addition, unprecedented use of antibiotics could substantially affect GM diversity.11 Increased prescription of antibiotics during pregnancy, which has been reported in several countries,12–14 could decrease GM diversity during pregnancy and may be deleterious for both maternal and fetal health. Furthermore, unnecessary and inappropriate use of antibiotics could induce teratogenicity, modulate GM composition, and contribute to the emergence of antimicrobial-resistant pathogens.15,16 Human GM has become a functional reservoir of antimicrobial resistance genes (ARGs)17 that could potentially be acquired by opportunistic pathogens.17,18 These pathogens could translocate from the gut to various body sites through fecal contamination, gut barrier penetration, and medical services (such as catheter replacement).19,20 Such pathogens could further complicate infections, especially in immune-compromised individuals (including pregnant women and infants),21,22 and stress health care resources. Bacterial pathogens carrying ARGs could affect ovum implantation, pregnancy sustention, and delivery, and they (...truncated)