Gelgie Aga E, Schneider Peleg, Citti Christine, Dordet-Frisoni Emilie, Gillespie Barbara E, Almeida Raúl A, Agga Getahun E, Amoah Yaa Serwaah, Shpigel Nahum Y, Kerro Dego Oudessa, Lysnyansky Inna
Department of Animal Science, The University of Tennessee, Knoxville, Tennessee, United States of America.
The Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel.
PLoS Pathog. 2024 Nov 12;20(11):e1012628. doi: 10.1371/journal.ppat.1012628. eCollection 2024 Nov.
Nucleases and 5' nucleotidase (5'-NT) play essential roles in cell biology and are often associated with bacterial virulence. In Mycoplasma spp., which have limited metabolic capacities and rely on nutrient availability, these enzymes are of significant importance for nucleotide salvage. This study explores the potential role of 2 membrane-associated lipoproteins, the major nuclease MnuA and 5'-NT, in Mycoplasma bovis mastitis. Mutants deficient in MnuA (mnuA::Tn) and in 5'-NT (0690::Tn) were identified through genome-wide transposon mutagenesis of M. bovis PG45 type strain and their fitness and virulence were assessed both in vitro, in axenic medium, and in vivo, using murine and cow mastitis models. The mnuA::Tn mutant demonstrated reduced nuclease activity, while 0690::Tn exhibited slow log-phase growth and impaired hydrolase activity towards nucleotides as well as deoxynucleotides (dAMP and dGMP). In comparison to the parent strain, the 0690::Tn mutant displayed markedly reduced fitness, as evidenced by a significant decrease or even absence in post-challenge mycoplasma counts in murine and cow mammary tissues, respectively. Moreover, the 0690::Tn mutant failed to induce mastitis in both experimental models. Conversely, the mnuA::Tn mutant induced inflammation in murine mammary glands, characterized by neutrophil infiltration and increased expression of major inflammatory genes. In cows, the mnuA::Tn was able to cause an increase in somatic cell counts in a manner comparable to the wild type, recruit neutrophils, and induce mastitis. Collectively, these findings provide complementary insights, revealing that disruption of 5'-NT significantly attenuated M. bovis pathogenicity, whereas a MnuA-deficient mutant retained the ability to cause mastitis.
核酸酶和5'核苷酸酶(5'-NT)在细胞生物学中发挥着重要作用,并且常常与细菌毒力相关。在代谢能力有限且依赖营养物质供应的支原体属中,这些酶对于核苷酸补救合成至关重要。本研究探讨了两种膜相关脂蛋白,即主要核酸酶MnuA和5'-NT,在牛支原体乳腺炎中的潜在作用。通过对牛支原体PG45型菌株进行全基因组转座子诱变,鉴定出MnuA缺陷型突变体(mnuA::Tn)和5'-NT缺陷型突变体(0690::Tn),并在体外无菌培养基以及体内使用小鼠和奶牛乳腺炎模型评估了它们的适应性和毒力。mnuA::Tn突变体的核酸酶活性降低,而0690::Tn在对数生长期生长缓慢,对核苷酸以及脱氧核苷酸(dAMP和dGMP)的水解酶活性受损。与亲本菌株相比,0690::Tn突变体的适应性显著降低,分别在小鼠和奶牛乳腺组织中的攻毒后支原体计数显著减少甚至缺失即可证明。此外,0690::Tn突变体在两种实验模型中均未能诱发乳腺炎。相反,mnuA::Tn突变体在小鼠乳腺中诱发炎症,其特征为中性粒细胞浸润和主要炎症基因表达增加。在奶牛中,mnuA::Tn能够以与野生型相当的方式导致体细胞计数增加,募集中性粒细胞并诱发乳腺炎。总的来说,这些发现提供了互补的见解,表明5'-NT的破坏显著减弱了牛支原体的致病性,而MnuA缺陷型突变体仍保留了引起乳腺炎的能力。