Maghembe Reuben S, Magulye Maximilian A K, Eilu Emmanuel, Sekyanzi Simon, Makaranga Abdalah, Mwesigwa Savannah, Katagirya Eric
Biological and Marine Sciences Unit, Faculty of Natural and Applied Sciences, Marian University College, P. O. Box 47, Bagamoyo, Tanzania; Department of Immunology and Molecular Biology, College of Health Sciences, Makerere University, P. O. Box 7072, Kampala, Uganda; Department of Microbiology and Immunology, Faculty of Biomedical Sciences, Kampala International University, Wester Campus, Ishaka, Uganda.; Microbiology Section, Department of Biological Sciences, University of Botswana, Private Bag 0704, Gaborone, Botswana.
Department of Immunology and Molecular Biology, College of Health Sciences, Makerere University, P. O. Box 7072, Kampala, Uganda.
Infect Genet Evol. 2024 Jun;120:105591. doi: 10.1016/j.meegid.2024.105591. Epub 2024 Apr 10.
Sepsis and multidrug resistance comprise a complex of factors attributable to mortality among intensive care unit (ICU) patients globally. Pathogens implicated in sepsis are diverse, and their virulence and drug resistance remain elusive. From a tertiary care hospital ICU in Uganda, we isolated a Citrobacter freundii strain RSM030 from a patient with sepsis and phenotypically tested it against a panel of 16 antibiotics including imipenem levofloxacin, cotrimoxazole and colistin, among others. We sequenced the organism's genome and integrated multilocus sequencing (MLST), PathogenFinder with Virulence Factor analyzer (VFanalyzer) to establish its pathogenic relevance. Thereafter, we combined antiSMASH and PRISM genome mining with molecular docking to predict biosynthetic gene clusters (BGCs), pathways, toxin structures and their potential targets in-silico. Finally, we coupled ResFinder with comprehensive antibiotic resistance database (CARD) to scrutinize the genomic antimicrobial resistance profile of the isolate. From PathogenFinder and MLST, this organism was confirmed to be a human pathogen (p = 0.843), sequence type (ST)150, whose virulence is determined by chromosomal type III secretion system (T3SS) (the injectosome) and plasmid-encoded type IV secretion system (T4SS), the enterobactin biosynthetic gene cluster and biofilm formation through the pgaABCD operon. Pathway and molecular docking analyses revealed that the shikimate pathway can generate a toxin targeting multiple host proteins including spectrin, detector of cytokinesis protein 2 (Dock2) and plasmalemma vesicle-associated protein (PLVAP), potentially distorting the host cell integrity. From phenotypic antibiotic testing, we found indeterminate results for amoxicillin/clavulanate and levofloxacin, with resistance to cotrimoxazole and colistin. Detailed genome analysis revealed chromosomal beta lactam resistance genes, i.e. blaCMY-79, blaCMY-116 and blaTEM-1B, along with multiple mutations of the lipopolysaccharide modifying operon genes PmrA/PmrB, pmrD, mgrA/mgrB and PhoP/PhoQ, conferring colistin resistance. From these findings, we infer that Citrobacter freundii strain RSM030 is implicated in sepsis and resistance to standard antibiotics, including colistin, the last resort.
脓毒症和多重耐药性是导致全球重症监护病房(ICU)患者死亡的复杂因素。与脓毒症相关的病原体多种多样,其毒力和耐药性仍不明确。我们从乌干达一家三级护理医院的ICU中,从一名脓毒症患者身上分离出弗氏柠檬酸杆菌菌株RSM030,并对其进行表型测试,检测其对包括亚胺培南、左氧氟沙星、复方新诺明和黏菌素等在内的16种抗生素的敏感性。我们对该菌株的基因组进行了测序,并结合多位点测序(MLST)、PathogenFinder和毒力因子分析仪(VFanalyzer)来确定其致病相关性。此后,我们将antiSMASH和PRISM基因组挖掘与分子对接相结合,以预测生物合成基因簇(BGCs)、途径、毒素结构及其潜在的计算机模拟靶点。最后,我们将ResFinder与综合抗生素耐药数据库(CARD)结合,以详细分析该分离株的基因组抗菌耐药谱。通过PathogenFinder和MLST分析,证实该菌株是一种人类病原体(p = 0.843),序列类型(ST)为150,其毒力由染色体III型分泌系统(T3SS)(注射体)和质粒编码的IV型分泌系统(T4SS)、肠杆菌素生物合成基因簇以及通过pgaABCD操纵子形成生物膜所决定。途径和分子对接分析表明,莽草酸途径可产生一种毒素,靶向多种宿主蛋白,包括血影蛋白、胞质分裂检测蛋白2(Dock2)和质膜囊泡相关蛋白(PLVAP),可能会破坏宿主细胞的完整性。从表型抗生素测试中,我们发现阿莫西林/克拉维酸和左氧氟沙星的结果不确定,对复方新诺明和黏菌素耐药。详细的基因组分析揭示了染色体β-内酰胺耐药基因,即blaCMY - 79、blaCMY - 116和blaTEM - 1B,以及脂多糖修饰操纵子基因PmrA/PmrB、pmrD、mgrA/mgrB和PhoP/PhoQ的多个突变,导致对黏菌素耐药。根据这些发现,我们推断弗氏柠檬酸杆菌菌株RSM030与脓毒症以及对包括黏菌素(最后一道防线)在内的标准抗生素耐药有关。