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Association of the Gut Microbiota Mobilome with Hospital Location and Birth Weight in Preterm Infants

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Association of the Gut Microbiota Mobilome with Hospital Location and Birth Weight in Preterm Infants nature publishing group Basic Science Investigation | Articles Association of the gut microbiota mobilome with hospital location and birth weight in preterm infants Anuradha Ravi1, Eva Lena F. Estensmo1, Trine M. L’Abée-Lund2, Steven L. Foley3, Bernhard Allgaier4, Camilia R. Martin5, Erika C. Claud6 and Knut Rudi1 BACKGROUND: The preterm infant gut microbiota is neonatal intensive care unit (NICU) microbial flora (1). In vulnerable to different biotic and abiotic factors. Although addition to this, very low birth weight (o1500 g) preterm the development of this microbiota has been extensively infants are affected by feeding intolerance and minimal studied, the mobilome—i.e. the mobile genetic elements intestinal growth (3). These factors threaten the development (MGEs) in the gut microbiota—has not been considered. of the commensal gut microbiota and are responsible for Therefore, the aim of this study was to investigate the delay in the succession of the adult gut microbiota, which may association of the mobilome with birth weight and hospital enhance the risk for sepsis (4) and necrotizing enterocolitis location in the preterm infant gut microbiota. (NEC) (5). Approximately 7% of very low birth weight infants METHODS: The data set consists of fecal samples from 62 develop NEC, with a mortality rate of 20–30% (2,6). This preterm infants with and without necrotizing enterocolitis multifactorial condition is based on premature birth, aberrant (NEC) from three different hospitals. We analyzed the gut intestinal microbiota development, and enteral feeding (2). microbiome by using 16S rRNA amplicon sequencing, shot- Although differences in the bacterial taxa of the gun metagenome sequencing, and quantitative PCR. Pre- gastrointestinal tract during preterm development have been dictive models and other data analyses were performed using extensively studied, the gene pool linked to mobile genetic MATLAB and QIIME. elements (MGEs) has not been investigated. Therefore, the RESULTS: The microbiota composition was significantly aim of this work was to investigate the mobilome (collection different between NEC-positive and NEC-negative infants of MGEs) of the gut microbiota in NEC-positive and and significantly different between hospitals. An operational NEC-negative preterm infants and their potential association taxanomic unit (OTU) showed strong positive and negative with birth weight and hospital location. correlation with NEC and birth weight, respectively, whereas The mobilome, in general, includes transposons, plasmids, none showed significance for mode of delivery. Metagenome and bacteriophages (7). Some of the major constituents of the analyses revealed high levels of conjugative plasmids with gut mobilome are conjugative plasmids (8). Conjugative MGEs and virulence genes. Results from quantitative PCR plasmids are self-replicating genetic elements that propagate showed that the plasmid signature genes were significantly in an infectious manner (8). They can harbor several different between hospitals and in NEC-positive infants. accessory functional elements that help to maintain long- CONCLUSION: Our results point toward an association of the term stability in a microbial population (9). In addition, two mobilome with hospital location in preterm infants. conjugative plasmid groups having identical replication machinery are incompatible in the same bacterial cell; hence, plasmids are identified based on their incompatibility (9). To date, 27 incompatibility groups have been defined (10). reterm infants constitute a unique patient population However, the most prominent are the incompatibility group F Pcompleting their development in an extra-uterine envir- (IncF) plasmids that are commonly found within the onment influenced by a concommitantly developing micro- Enterobacteriaceae family (11). These plasmids have been biome. Further, this patient group largely acquires its initial detected in bacteria from several human and animal sources. microbiota from within the hospital environment. As preterm IncF conjugative plasmids contain an assortment of other infants spend many months in the hospital, their health is MGEs and virulence genes (12). Plasmid-mediated hospital- dependent on different factors to which they are exposed, acquired infections have been previously reported, explaining such as chemicals (1), parenteral feeding (2), and exposure to the influence of conjugal transfer of virulence factors and 1Chemistry, Biotechnology and Food Science Department (IKBM), Norwegian University of Life Sciences, Campus Ås, Ås, Norway; 2Department of Food Safety and Infection Biology, Norwegian University of Life Sciences, Campus Adamstuen, Oslo, Norway; 3Division of Microbiology, U.S. Food and Drug Administration, National Center for Toxicology Research, Jefferson, Arkansas; 4Department of Pediatrics, NorthShore University HealthCenter, Evanston, Illinois; 5Department of Neonatology and Division of Translational Research, Beth Israel Deaconess Medical Center, Boston, Massachusetts; 6Departments of Pediatrics and Medicine, Biological Sciences Division, The University of Chicago, Chicago, Illinois. Correspondence: Knut Rudi ([email protected]) Received 5 August 2016; accepted 4 June 2017; advance online publication 2 August 2017. doi:10.1038/pr.2017.146 Copyright © 2017 International Pediatric Research Foundation, Inc. Volume 82 | Number 5 | November 2017 Pediatric RESEARCH 829 Articles | Ravi et al. 16S rRNA sequencing and analysis 16S rRNA data set 6000seq/ id=55 Metagenome analysis Sample n=134 d=58 Selected dataset (B-2; C-2; E-1) NEC cohort id=62 Shotgun metagenome dataset n=160 id=5; n=15 d=120 Quantitative PCR analysis Identify specific Functional OTU sequences abundance of Int1 genes id=62; n=160 De novo assembly of reads into contigs Screen for signature genes RepA Abundance of antibiotic Analyze contigs for resistance genes YigB plasmid related genes Relative quantification Screen plasmid signature genes Figure 1. Workflow of the experimental setup. B, Boston; C, Chicago; d, duplicate samples; E, Evanston; id, number of patients; n, number of samples included. inducement of bacterial biofilms (13,14). Virulence traits infants with NEC showed NEC symptoms that were more severe associated with MGEs include bacterial toxins (15), secretion than Bell’s stage II, with mild to moderate systemic illness and pneumatosis intestinalis. The infants were recruited from three systems (16), and hemolysins (14). These properties can different hospitals in the USA: Beth Israel Hospital in Boston, MA transform the characteristics of the host cell. (n = 24); Comer Children’s Hospital at The University of Chicago in Integrons are accessory components of conjugative plas- Chicago, IL (n = 29); and NorthShore University HealthSystem mids (17). They are genetic elements capable of integration Hospital in Evanston, IL (n = 9). These infants resided in the NICU of the respective hospitals. In total, the study consists of 23 NEC- and expression of genetic cassettes by an overall common positive infants and 39 NEC-negative infants. The children were promoter (17,18). The integron consists of three main parts: treated individually, and not as matched case controls, because of the an integrase (int1) gene that helps in the integration of limitations of the data set related to NEC sampling. specific gene cassettes; an attachment (att1) site into which There were 63 samples from NEC-positive infants, including 51 the gene cassettes are integrated; and the common promoter samples from the longitudinal data sets. There were 97 samples from NEC-negative infants, where 73 samples were from longitudinal data (Pc) for expression of the gene cassettes (19). sets, with samples from 29 infants being collected over a 3-day In this study, we investigated the intestinal microbiome of period. Informed consent was obtained from the preterm infants’ very low birth weight preterm infants from three neonatal parents for fecal sample collection and storage. The samples were intensive care units. Amplicon sequencing was used to collected directly from the diaper into the collection tube using the wooden end of a sterile cotton swab. The samples were immediately identify compositional signatures in the microbiota composi- frozen at − 80 °C until processed. The samples were sent to Genetic tion. Then, full metagenome deep sequencing was used for Analysis, Ås, Norway, for longtime storage and DNA extraction. analyzing the phylogeny and genetic background of MGEs in selected samples. Finally, quantitative PCR was used to study DNA Extraction the prevalence and quantity of plasmid signature sequences DNA was isolated from 160 samples using an automated protocol of MagNA Pure Compact System (Roche Applied Science, Basel, and their association with MGEs. Switzerland). DNA from a subset of samples in the data set was also manually extracted using the QIAamp DNA Stool mini kit (Qiagen, METHODS Venlo, Netherlands). These were termed duplicates. Fifty mg of frozen fecal sample was dissolved in 1 ml extraction buffer [50 mM Workflow Tris (pH 7.4), 100 mM EDTA (pH 8.0), and 400 mM NaCl, 0.5% SDS] A workflow of the experimental design and the total number of containing 20 μl proteinase K (20 mg/ml), and 500 μl of 0.1-mm- samples used are shown in Figure 1. diameter zirconia/silica beads (BioSpec Products, Bartlesville, OK) was added to the extraction tubes and a Mini-Beadbeater-16 Cohort Description (BioSpec Products) was used to lyse the microbial cells. The lysed Table 1 provides
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