Carter Michelle Qiu, Quiñones Beatriz, Laniohan Nicole, Carychao Diana, Pham Antares, He Xiaohua, Cooley Michael
Produce Safety and Microbiology Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, CA, United States.
Foodborne Toxin Detection and Prevention Research Unit, U.S. Department of Agriculture, Agricultural Research Service, Western Regional Research Center, Albany, CA, United States.
Front Microbiol. 2023 Sep 26;14:1214081. doi: 10.3389/fmicb.2023.1214081. eCollection 2023.
Shiga toxin-producing (STEC) consists of diverse strains differing in genetic make-up and virulence potential. To better understand the pathogenicity potential of STEC carried by the wildlife, three STEC and one strains isolated from wild birds near a major agricultural region in California were selected for comparative pathogenomic analyses. Three American crow () strains, RM9088, RM9513, and RM10410, belonging to phylogroup A with serotypes O109:H48, O9:H30, and O113:H4, respectively, and a red-winged blackbird () strain RM14516 in phylogroup D with serotype O17:H18, were examined. Shiga toxin genes were identified in RM9088 (), RM10410 ( + ), and RM14516 (). Unlike STEC O157:H7 strain EDL933, none of the avian STEC strains harbored the pathogenicity islands OI-122, OI-57, and the locus of enterocyte effacement, therefore the type III secretion system biogenesis genes and related effector genes were absent in the three avian STEC genomes. Interestingly, all avian STEC strains exhibited greater (RM9088 and RM14516) or comparable (RM10410) cytotoxicity levels compared with EDL933. Comparative pathogenomic analyses revealed that RM9088 harbored numerous genes encoding toxins, toxins delivery systems, and adherence factors, including heat-labile enterotoxin, serine protease autotransporter toxin Pic, type VI secretion systems, protein adhesin Paa, fimbrial adhesin K88, and colonization factor antigen I. RM9088 also harbored a 36-Kb high pathogenicity island, which is related to iron acquisition and pathogenicity in spp. Strain RM14516 carried an acid fitness island like the one in EDL933, containing a nine gene cluster involved in iron acquisition. Genes encoding extracellular serine protease EspP, subtilase cytotoxin, F1C fimbriae, and inverse autotransporter adhesin IatC were only detected in RM14516, and genes encoding serine protease autotransporter EspI and P fimbriae were only identified in RM10410. Although all curli genes were present in avian STEC strains, production of curli fimbriae was only detected for RM9088 and RM14516. Consistently, strong, moderate, and little biofilms were observed for RM9088, RM14516, and RM10410, respectively. Our study revealed novel combinations of virulence factors in two avian strains, which exhibited high level of cytotoxicity and strong biofilm formation. Comparative pathogenomics is powerful in assessing pathogenicity and health risk of STEC strains.
产志贺毒素大肠杆菌（STEC）由基因组成和毒力潜力不同的多种菌株构成。为了更好地了解野生动物携带的STEC的致病潜力，从加利福尼亚一个主要农业地区附近的野生鸟类中分离出三株STEC和一株其他菌株，用于比较病原基因组分析。对三株美洲鸦（Corvus brachyrhynchos）菌株RM9088、RM9513和RM10410进行了检测，它们分别属于A群，血清型为O109:H48、O9:H30和O113:H4；还有一株红翅黑鹂（Agelaius phoeniceus）菌株RM14516，属于D群，血清型为O17:H18。在RM9088（stx2e）、RM10410（stx2 + stx1）和RM14516（stx2）中鉴定出了志贺毒素基因。与STEC O157:H7菌株EDL933不同，所有禽源STEC菌株均未携带致病岛OI - 122、OI - 57和肠细胞脱落位点，因此在这三株禽源STEC基因组中不存在III型分泌系统生物发生基因和相关效应基因。有趣的是，与EDL933相比，所有禽源STEC菌株均表现出更高（RM9088和RM14516）或相当（RM10410）的细胞毒性水平。比较病原基因组分析表明，RM9088含有许多编码毒素、毒素递送系统和黏附因子的基因，包括不耐热肠毒素、丝氨酸蛋白酶自转运毒素Pic、VI型分泌系统、蛋白质黏附素Paa、菌毛黏附素K88和定植因子抗原I。RM9088还含有一个36-Kb的高致病岛，这与大肠杆菌属物种中的铁获取和致病性有关。菌株RM14516携带一个与EDL933中类似的酸适应性岛，包含一个参与铁获取的九个基因簇。仅在RM14516中检测到编码细胞外丝氨酸蛋白酶EspP、枯草杆菌蛋白酶细胞毒素、F1C菌毛和反向自转运黏附素IatC的基因，仅在RM10410中鉴定出编码丝氨酸蛋白酶自转运体EspI和P菌毛的基因。尽管所有卷曲菌毛基因均存在于禽源STEC菌株中，但仅在RM9088和RM14516中检测到卷曲菌毛的产生。一致地，分别在RM9088、RM14516和RM10410中观察到强、中和弱生物膜形成。我们的研究揭示了两种禽源菌株中毒力因子的新组合，它们表现出高水平的细胞毒性和强烈的生物膜形成。比较病原基因组学在评估STEC菌株的致病性和健康风险方面具有强大作用。
