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Metatranscriptomic Analysis Reveals Active Bacterial Communities in Diabetic Foot Infections

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Metatranscriptomic Analysis Reveals Active Bacterial Communities in Diabetic Foot Infections fmicb-11-01688 July 20, 2020 Time: 12:22 # 1 ORIGINAL RESEARCH published: 22 July 2020 doi: 10.3389/fmicb.2020.01688 Metatranscriptomic Analysis Reveals Active Bacterial Communities in Diabetic Foot Infections Fatemah Sadeghpour Heravi1, Martha Zakrzewski2, Karen Vickery1, Matthew Malone3,4,5 and Honghua Hu1* 1 Surgical Infection Research Group, Faculty of Medicine and Health Sciences, Macquarie University, Sydney, NSW, Australia, 2 QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia, 3 Infectious Diseases and Microbiology, School of Medicine, Western Sydney University, Sydney, NSW, Australia, 4 Liverpool Hospital, South Western Sydney LHD, Sydney, NSW, Australia, 5 Liverpool Diabetes Collaborative Research Unit, Ingham Institute for Applied Medical Research, Sydney, NSW, Australia Despite the extended view of the composition of diabetic foot infections (DFIs), little is known about which transcriptionally active bacterial communities are pertinent to infection, and if any differences are associated with increased infection severity. We applied a RNA sequencing approach to analyze the composition, function, and pathogenicity of the active bacterial communities in DFIs. Taxonomic profiling of bacterial transcripts revealed the presence of 14 bacterial phyla in DFIs. The abundance Edited by: Qi Zhao, of the Spiroplasma, Vibrio, and Mycoplasma were significantly different in different Liaoning University, China infection severities (P < 0.05). Mild and severe stages of infections were dominated Reviewed by: by Staphylococcus aureus and Porphyromonas asaccharolytica, respectively. A total of Patrick R. M. Harnarayan, The University of the West Indies 132 metabolic pathways were identified of which ribosome and thiamin being among the at St. Augustine, Trinidad and Tobago most highly transcribed pathways. Moreover, a total of 131 antibiotic resistance genes, Maria José Saavedra, primarily involved in the multidrug efflux pumps/exporters, were identified. Furthermore, Universidade de Trás-os-Montes e Alto Douro, Portugal iron acquisition systems (synthesize and regulation of siderophores) and pathways *Correspondence: involved in the synthesis and regulation of cell-surface components associated with Honghua Hu adhesion, colonization, and movement of bacterial cells were the most common [email protected] virulence factors. These virulence factors may help bacteria compete for scares Specialty section: resources and survive the host wound proteases. Characterization of transcriptionally This article was submitted to active bacterial communities can help to provide an understanding of the role of key Systems Microbiology, a section of the journal pathogens in the development of DFIs. Such information can be clinically useful allowing Frontiers in Microbiology replacement of DFIs empirical therapy with targeted treatment. Received: 22 May 2020 Accepted: 29 June 2020 Keywords: diabetic foot infection, RNA sequencing, metatranscriptomics, active bacterial community, resistome, virulence factors Published: 22 July 2020 Citation: Heravi FS, Zakrzewski M, INTRODUCTION Vickery K, Malone M and Hu H (2020) Metatranscriptomic Analysis Reveals Active Bacterial Communities Diabetic foot infections (DFIs) are a frequent cause of hospitalization and typically precede events in Diabetic Foot Infections. such as lower extremity amputation (Lavery et al., 2003). Traditional approaches to identify Front. Microbiol. 11:1688. pathogens colonized in DFIs have relied on culture-based methods that are limited to detect doi: 10.3389/fmicb.2020.01688 bacterial species grown under standard laboratory conditions (Heravi et al., 2020). Frontiers in Microbiology| www.frontiersin.org 1 July 2020| Volume 11| Article 1688 fmicb-11-01688 July 20, 2020 Time: 12:22 # 2 Heravi et al. Metatranscriptomics of Diabetic Foot Infection Over the last decade, several studies have identified that Waltham, MA, United States) for 24 h at 4◦C and then stored at diabetic foot ulcers were composed of a complex bacterial −80◦C until processed. community consisting of aerobes, anaerobes, fastidious, and unculturable microorganisms using 16S rRNA sequencing (Smith Sample Pretreatment et al., 2016; Gardiner et al., 2017). The 16S rRNA approach Infected tissue specimens (<25 mg) were homogenized in is limited to genomically present but transcriptionally inactive 1 ml TRIzol reagent (Invitrogen, Carlsbad, CA, United States) bacterial communities. It also does not provide insight into the using TissueRuptor II (Qiagen, Hilden, Germany) at 230 V, potential or actual function of the bacterial community in DFIs. 50/60 Hz for 10 s. High-throughput RNA sequencing or metatranscriptomic analysis is a promising tool to obtain insights into RNA Extraction the functionality of active bacterial communities. The above pretreated tissue samples (<25 mg) were Metatranscriptomics has also addressed the limitation of incubated in 1 ml TRIzol reagent for 5 min prior to further microarray assays such as unspecific hybridization signals homogenization using 0.1 and 0.5 mm beads in a FastPrep- (Zhao et al., 2016). 24 instrument (MP Biomedicals, Irvine, CA, United States) The composition and function of the active bacterial with a velocity of 5 m/s for 1 min while sitting on dry communities in DFIs can provide a clue for understanding the ice to break the bacterial cell wall. TRIzol R Plus RNA actual role of microorganisms in infection progression and the Purification Kit (Invitrogen, Carlsbad, CA, United States) improvement of therapeutic approaches. To the best of our was used to extract high-quality RNA from homogenized knowledge, this is the first study applying an RNA sequencing tissue samples. Extracted RNA was further treated with approach to explore the composition, function, and virulence TURBO DNase (Invitrogen, Carlsbad, CA, United States) factors of the transcriptionally active bacteria in DFIs. and purified by AMPure XP beads (Beckman Coulter Life Sciences, San Jose, CA, United States) according to the manufacturer’s instructions. MATERIALS AND METHODS RNA Integrity, Synthesis of cDNA, and Ethics Statement Illumina Sequencing This study was approved by the South West Sydney Local Health Quality and integrity of extracted RNA were evaluated in District Research and Ethics Committee (HREC/14/LPOOL/487, an Agilent 2100 Bioanalyzer system using microfluidics-based SSA/14/LPOOL/489) and Macquarie University Human electrophoresis on microfluidic chips (Agilent Technologies, Ethics Committee (Reference No. 5201500839). All the Santa Clara, CA, United States) which produced an RNA integrity experiments were performed in accordance with relevant number (RIN) as an output. Illumina whole transcriptome guidelines and regulations. Informed consent has been library preparation with rRNA depletion was performed using obtained for this study. the Illumina Ribo-Zero Gold Epidemiology kit (Illumina Inc., San Diego, CA, United States) on 16 selected high-quality Patient Population RNA samples. The RNA sequencing was run on one Illumina In this prospective study, 43 consecutive patients aged over NovaSeq 6000 S4 flow cell (300 Cycle) by the Australian Genome 18 years presenting to the Liverpool Hospital High-Risk Research Facility to achieve >150 million pair-end reads of 150 Foot Service with a clinically diagnosed DFI were enrolled nucleotides per sample. over a 6-month period. Infection severity was determined using the International Working Group of the Diabetic Foot Processing of Metatranscriptome Data (IWGDF), Perfusion, Extent, Depth, Infection and Sensation Sequencing reads were passed through the FastQC quality (PEDIS) classification system, and patients were assigned control pipeline Version 0.11.7 (Andrews, 2010) to visualize accordingly (PEDIS 2 refers to mild infection, PEDIS 3 refers their quality. Sequencing reads were trimmed and quality-filtered to moderate infection, PEDIS 4 refers to severe infection) with Trimmomatic tool version 0.39 (LEADING:5, TRAILING:5, (Lipsky et al., 2016). Since RNA sequencing approach requires SLIDINGWINDOW = 4:15, MINLEN = 50) (Bolger et al., RNA with high quality and integrity, after RNA extraction 2014). To filter human sequencing reads, trimmed reads were from all of the clinical samples and initial assessment, 16 mapped to the human reference genome using ultrafast universal samples that had high-quality and integrity RNA were selected RNA-seq aligner (STAR v2.5.2a, human reference: GRCh37 for RNA sequencing. genome including transcript annotation) (Dobin et al., 2013) and Burrows-Wheeler Alignment (BWA-mem version 0.7.15, human Sample Collection reference: GRCh38) (Li and Durbin, 2009). Putative non-human After the DFI ulcer was cleaned with sterile 0.9% NaCl, a reads were then mapped to ribosome RNA databases (SILVA sterile single-use punch with a circular hollow blade was rotated 16S, 23S, 28S, 18S rRNA, rfam 5S rRNA) using SortMeRNA around the affected area, and then the sharp debridement was v2.1 to identify and remove ribosomal RNA sequences (Kopylova collected by disposable forceps and preserved immediately in a et al., 2012). Putative bacterial mRNA was the target for further 2 ml RNAlater stabilization solution (Thermo Fisher Scientific, analyses (Figure 1). Frontiers in Microbiology| www.frontiersin.org 2 July 2020| Volume 11| Article 1688 fmicb-11-01688 July 20, 2020 Time: 12:22 # 3 Heravi et al. Metatranscriptomics of Diabetic Foot Infection FIGURE 1 | Overview of the metatranscriptome pipeline applied in this study. Bacterial Taxonomic Classification,
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