Department of Biology and Wildlife Diseases, Faculty of Veterinary Hygiene and Ecology, University of Veterinary Sciences Brno, Brno, Czech Republic.
CEITEC, University of Veterinary Sciences Brno, Brno, Czech Republic.
Appl Environ Microbiol. 2023 Aug 30;89(8):e0037123. doi: 10.1128/aem.00371-23. Epub 2023 Aug 14.
The operon encoding short-chain fructooligosaccharide (scFOS) utilization enables bacteria of the family to grow and be sustained in environments where they would struggle to survive. Despite several cases of the detection of the operon in isolates of avian and equine origins, its global distribution in bacterial genomes remains unknown. The presence of the plasmid-harbored operon among resistant bacteria may promote the spread of antibiotic resistance. A collection of 11,538 antimicrobial-resistant isolates from various sources was screened for the gene encoding the scFOS transporter. Out of 307 -positive isolates, 80% of them originated from sources not previously linked to (humans, wastewater, and animals). The chromosomally harbored operon was detected in 163/237 isolates subjected to whole-genome sequencing. In the remaining 74 isolates, the operon was carried by plasmids. Further analyses focusing on the isolates with a plasmid-harbored operon showed that the operon was linked to various incompatibility (Inc) groups, including the IncHI1, IncF-type, IncK2, IncI1, and IncY families. Long-read sequencing of representative plasmids showed the colocalization of genes with antibiotic resistance genes (ARGs) in IncHI1 (containing a multidrug resistance region), IncK2 (), IncI1 [ and (A)], and IncY [, , , and (A)] plasmids, while IncF-type plasmids had no ARGs but coharbored virulence-associated genes. Despite the differences in the locations and structures of the operons, all isolates except one were proven to utilize scFOSs. In this study, we show that the operon and its spread are not strictly bound to one group of plasmids, and therefore, it should not be overlooked. It was believed that members of the family are unable to grow under conditions with short-chain fructooligosaccharides as the only source of carbon. Nevertheless, the first Escherichia coli isolate from chicken intestine was able to utilize these sugars owing to the chromosomally harbored operon. Studies on E. coli isolates from horses discovered the horizontal transfer of the operon on IncHI1 plasmids along with genes for antibiotic resistance. The first plasmid detected was pEQ1, originating from the feces of a hospitalized horse in the Czech Republic. Follow-up studies also revealed the dissemination of the IncHI1 plasmid-harbored operon in the Netherlands, Germany, Denmark, and France among healthy horses. Despite several cases of detection of the operon, its global distribution in bacterial genomes remains unknown. The operon possibly plays a role in the adaptation of plasmids among resistant bacteria and therefore may promote the spread of antibiotic resistance.
操纵子编码短链果聚糖（scFOS）利用使家族的细菌能够在它们难以生存的环境中生长和维持。尽管已经在禽源和马源的分离株中检测到了操纵子，但它在细菌基因组中的全球分布仍然未知。在耐药菌中，携带质粒的操纵子的存在可能会促进抗生素耐药性的传播。从各种来源筛选了 11538 株抗微生物耐药性的分离株，以检测编码 scFOS 转运蛋白的基因。在 307 个阳性分离株中，有 80%来自以前与（人类、废水和动物）无关的来源。在进行全基因组测序的 237 个分离株中检测到了染色体上的操纵子。在其余的 74 个分离株中，操纵子由质粒携带。对携带质粒的操纵子的分离株进行进一步分析表明，操纵子与各种不相容性（Inc）群有关，包括 IncHI1、IncF 型、IncK2、IncI1 和 IncY 家族。代表性质粒的长读测序显示，IncHI1 中（含有多药耐药区）的抗生素耐药基因（ARGs）与 基因共定位，IncK2 中 基因与 IncI1 [和（A）]中 基因共定位，IncY [、、、和（A）]中 基因与 IncY 共定位质粒，而 IncF 型质粒没有 ARGs，但共同携带毒力相关基因。尽管操纵子的位置和结构存在差异，但除一个分离株外，所有分离株均被证明能够利用 scFOS。在这项研究中，我们表明，操纵子及其传播并不严格局限于一组质粒，因此不应被忽视。人们认为，家族成员在以短链果聚糖为唯一碳源的条件下无法生长。然而，第一株来自鸡肠道的大肠杆菌分离株能够利用这些糖，这要归功于染色体上的操纵子。对来自马的大肠杆菌分离株的研究发现，IncHI1 质粒上的 操纵子与抗生素耐药基因一起发生水平转移。检测到的第一个质粒是 pEQ1，它来自捷克共和国住院马的粪便。后续研究还揭示了在荷兰、德国、丹麦和法国，健康马中 IncHI1 质粒携带的 操纵子的传播。尽管已经检测到几个操纵子，但它在细菌基因组中的全球分布仍然未知。操纵子可能在耐药菌中质粒的适应中发挥作用，因此可能会促进抗生素耐药性的传播。
