Fahimipour Ashkaan K, Ben Mamaar Sarah, McFarland Alexander G, Blaustein Ryan A, Chen Jing, Glawe Adam J, Kline Jeff, Green Jessica L, Halden Rolf U, Van Den Wymelenberg Kevin, Huttenhower Curtis, Hartmann Erica M
Biology and the Built Environment Center, University of Oregon, Eugene, Oregon, USA.
Department of Civil and Environmental Engineering, Northwestern University, Evanston, Illinois, USA.
mSystems. 2018 Dec 11;3(6). doi: 10.1128/mSystems.00200-18. eCollection 2018 Nov-Dec.
Humans purposefully and inadvertently introduce antimicrobial chemicals into buildings, resulting in widespread compounds, including triclosan, triclocarban, and parabens, in indoor dust. Meanwhile, drug-resistant infections continue to increase, raising concerns that buildings function as reservoirs of, or even select for, resistant microorganisms. Support for these hypotheses is limited largely since data describing relationships between antimicrobials and indoor microbial communities are scant. We combined liquid chromatography-isotope dilution tandem mass spectrometry with metagenomic shotgun sequencing of dust collected from athletic facilities to characterize relationships between indoor antimicrobial chemicals and microbial communities. Elevated levels of triclosan and triclocarban, but not parabens, were associated with distinct indoor microbiomes. Dust of high triclosan content contained increased Gram-positive species with diverse drug resistance capabilities, whose pangenomes were enriched for genes encoding osmotic stress responses, efflux pump regulation, lipid metabolism, and material transport across cell membranes; such triclosan-associated functional shifts have been documented in laboratory cultures but not yet from buildings. Antibiotic-resistant bacterial isolates were cultured from all but one facility, and resistance often increased in buildings with very high triclosan levels, suggesting links between human encounters with viable drug-resistant bacteria and local biocide conditions. This characterization uncovers complex relationships between antimicrobials and indoor microbiomes: some chemicals elicit effects, whereas others may not, and no single functional or resistance factor explained chemical-microbe associations. These results suggest that anthropogenic chemicals impact microbial systems in or around buildings and their occupants, highlighting an emergent need to identify the most important indoor, outdoor, and host-associated sources of antimicrobial chemical-resistome interactions. The ubiquitous use of antimicrobial chemicals may have undesired consequences, particularly on microbes in buildings. This study shows that the taxonomy and function of microbes in indoor dust are strongly associated with antimicrobial chemicals-more so than any other feature of the buildings. Moreover, we identified links between antimicrobial chemical concentrations in dust and culturable bacteria that are cross-resistant to three clinically relevant antibiotics. These findings suggest that humans may be influencing the microbial species and genes that are found indoors through the addition and removal of particular antimicrobial chemicals.
人类有意或无意地将抗菌化学物质引入建筑物,导致室内灰尘中广泛存在三氯生、三氯卡班和对羟基苯甲酸酯等化合物。与此同时,耐药性感染持续增加,引发了人们对建筑物成为耐药微生物储存库甚至对其进行选择的担忧。由于描述抗菌剂与室内微生物群落之间关系的数据很少,对这些假设的支持在很大程度上受到限制。我们将液相色谱-同位素稀释串联质谱与从体育设施收集的灰尘的宏基因组鸟枪法测序相结合,以表征室内抗菌化学物质与微生物群落之间的关系。三氯生和三氯卡班(而非对羟基苯甲酸酯)的含量升高与不同的室内微生物群落有关。三氯生含量高的灰尘中革兰氏阳性菌种类增加,具有多种耐药能力,其泛基因组富含编码渗透应激反应、外排泵调节、脂质代谢和跨细胞膜物质运输的基因;这种与三氯生相关的功能变化在实验室培养中已有记录,但尚未在建筑物中发现。除一个设施外,所有设施都培养出了耐抗生素细菌分离株,在三氯生含量非常高的建筑物中,耐药性通常会增加,这表明人类接触有活力的耐药细菌与当地的杀菌剂状况之间存在联系。这一特征揭示了抗菌剂与室内微生物群落之间的复杂关系:有些化学物质会产生影响,而有些则可能不会,而且没有单一的功能或耐药因素能够解释化学物质与微生物之间的关联。这些结果表明,人为化学物质会影响建筑物内或周围及其居住者的微生物系统,凸显了迫切需要确定抗菌化学物质-耐药基因组相互作用的最重要的室内、室外和宿主相关来源。抗菌化学物质的广泛使用可能会产生不良后果,尤其是对建筑物中的微生物。这项研究表明,室内灰尘中微生物的分类和功能与抗菌化学物质密切相关,比建筑物的任何其他特征都更为密切。此外,我们确定了灰尘中抗菌化学物质浓度与对三种临床相关抗生素具有交叉耐药性的可培养细菌之间的联系。这些发现表明,人类可能通过添加和去除特定的抗菌化学物质来影响室内发现的微生物种类和基因。