Pathogenicity of psychrotolerant strains of Antarctic Pseudogmynoascus fungi reveals potential opportunistic profiles

Eldon Carlos Queres Gomes , Vívian Nicolau Gonçalves , Marliete Carvalho da Costa , Gustavo José Cota de Freitas , Daniel Assis Santos , Susana Johann , Jefferson Bruno Soares Oliveira , Tatiane Alves da Paixão , Peter Convey , Luiz Henrique Rosa
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Abstract

Recent studies have demonstrated the presence of fungal taxa in the extreme ecosystems of Antarctica that are known to opportunistically infect humans and animals. Among these are members of the genus Pseudogymnoascus, including some that are genetically similar to P. destructans, known to be pathogenic to bats. We evaluated the in vitro and in vivo pathogenic potential of 11 Pseudogymnoascus spp. strains recovered from Antarctica. All strains were able to grow at temperatures up to 28 °C and displayed in vitro pathogenicity through hemolytic activity, growth at different pH levels, production of hydrolytic enzymes, spore diameters, tolerance to oxidative stress, hypoxia, and halotolerance. Among them, Pseudogymnoascus sp. UFMG 8532 exhibited strong in vitro pathogenicity and in preliminary in vivo assay killed 100 % of Tenebrio molitor larvae within one day. The pathogenicity of the same strain was also tested using immunosuppressed BALB/c mouse models. Survival of BALB/c mice was affected, with oscillations between weight gain and loss, and impacts on sensory function, reflexes and autonomic function. Histopathological data from the organs of infected mice showed evidence of inflammatory processes, with numerous neutrophils, a small number of macrophages, fluid accumulation inside the lungs and intense hyperemia. Our results indicate that Antarctic Pseudogymnoascus spp. strains obtained from various substrates/habitats in maritime Antarctica may possess intrinsic virulence factors and pathogenic potential for immunosuppressed animals and humans in the region. Given that the Antarctic environment is an important reservoir for Pseudogymnoascus species, which display growth performance across a range of temperatures, it is possible that increasing temperatures in the maritime Antarctic could activate dormant genes or biochemical pathways, select virulent species and/or strains, and facilitate their spread within and beyond the region. The ability of Pseudogymnoascus species to grow slowly even at 28°C, coupled with their potential in vitro and in vivo virulence factors, suggests that these fungi might be undergoing an opportunistic transition due to the effects of climate change on the Antarctic Peninsula.
南极伪膜真菌精神耐受菌株的致病性揭示了潜在的机会主义特征
最近的研究表明,在南极洲的极端生态系统中存在着真菌类群,这些真菌类群可伺机感染人类和动物。其中包括假蝙蝠疫霉属(Pseudogymnoascus)的成员,包括一些与已知对蝙蝠具有致病性的毁灭蝙蝠疫霉(P. destructans)基因相似的成员。我们评估了从南极洲发现的 11 株假丝酵母菌的体外和体内致病潜力。所有菌株都能在最高 28 °C 的温度下生长,并通过溶血活性、在不同 pH 值水平下的生长、水解酶的产生、孢子直径、对氧化应激的耐受性、缺氧和耐卤性表现出体外致病性。其中,Pseudogymnoascus sp. UFMG 8532 具有很强的体外致病性,在初步体内试验中,它能在一天内杀死 100% 的褐斑天牛幼虫。同一菌株的致病性还通过免疫抑制 BALB/c 小鼠模型进行了测试。BALB/c 小鼠的存活率受到影响,体重在增加和减少之间摇摆,感觉功能、反射和自主神经功能也受到影响。受感染小鼠器官的组织病理学数据显示了炎症过程的证据,其中包括大量中性粒细胞、少量巨噬细胞、肺内积液和严重充血。我们的研究结果表明,从南极海域各种基质/栖息地获得的南极假丝酵母菌株可能具有内在毒力因子,对该地区免疫抑制动物和人类具有致病潜力。鉴于南极环境是假丝虫物种的重要贮藏地,而假丝虫物种在各种温度下都能生长,因此南极海域温度升高可能会激活休眠基因或生化途径,选择毒性物种和/或菌株,并促进其在该地区内外的传播。假革囊真菌即使在 28°C 的温度下也能缓慢生长,再加上其潜在的体外和体内毒力因子,表明这些真菌可能正在经历南极半岛气候变化影响下的机会性转变。
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