Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Gustav Wieds Vej 14, 8000 Aarhus, Denmark.
Department Infectious Diseases, Aarhus University Hospital, Palle Juul-Jensens bvld 99, 8200 Aarhus N, Denmark.
Nucleic Acids Res. 2024 Feb 28;52(4):1575-1590. doi: 10.1093/nar/gkae034.
Many bacteria form biofilms to protect themselves from predators or stressful environmental conditions. In the biofilm, bacteria are embedded in a protective extracellular matrix composed of polysaccharides, proteins and extracellular DNA (eDNA). eDNA most often is released from lysed bacteria or host mammalian cells, and it is the only matrix component most biofilms appear to have in common. However, little is known about the form DNA takes in the extracellular space, and how different non-canonical DNA structures such as Z-DNA or G-quadruplexes might contribute to its function in the biofilm. The aim of this study was to determine if non-canonical DNA structures form in eDNA-rich staphylococcal biofilms, and if these structures protect the biofilm from degradation by nucleases. We grew Staphylococcus epidermidis biofilms in laboratory media supplemented with hemin and NaCl to stabilize secondary DNA structures and visualized their location by immunolabelling and fluorescence microscopy. We furthermore visualized the macroscopic biofilm structure by optical coherence tomography. We developed assays to quantify degradation of Z-DNA and G-quadruplex DNA oligos by different nucleases, and subsequently investigated how these enzymes affected eDNA in the biofilms. Z-DNA and G-quadruplex DNA were abundant in the biofilm matrix, and were often present in a web-like structures. In vitro, the structures did not form in the absence of NaCl or mechanical shaking during biofilm growth, or in bacterial strains deficient in eDNA or exopolysaccharide production. We thus infer that eDNA and polysaccharides interact, leading to non-canonical DNA structures under mechanical stress when stabilized by salt. We also confirmed that G-quadruplex DNA and Z-DNA was present in biofilms from infected implants in a murine implant-associated osteomyelitis model. Mammalian DNase I lacked activity against Z-DNA and G-quadruplex DNA, while Micrococcal nuclease could degrade G-quadruplex DNA and S1 Aspergillus nuclease could degrade Z-DNA. Micrococcal nuclease, which originates from Staphylococcus aureus, may thus be key for dispersal of biofilm in staphylococci. In addition to its structural role, we show for the first time that the eDNA in biofilms forms a DNAzyme with peroxidase-like activity in the presence of hemin. While peroxidases are part of host defenses against pathogens, we now show that biofilms can possess intrinsic peroxidase activity in the extracellular matrix.
许多细菌形成生物膜以保护自己免受捕食者或压力环境条件的影响。在生物膜中,细菌嵌入由多糖、蛋白质和细胞外 DNA (eDNA)组成的保护性细胞外基质中。eDNA 最常从裂解的细菌或宿主哺乳动物细胞中释放出来,而且它是唯一似乎大多数生物膜都共有的基质成分。然而,人们对细胞外空间中 DNA 的形式知之甚少,也不知道不同的非典型 DNA 结构,如 Z-DNA 或 G-四链体,如何有助于其在生物膜中的功能。本研究的目的是确定富含 eDNA 的葡萄球菌生物膜中是否形成非典型 DNA 结构,以及这些结构是否能保护生物膜免受核酸酶的降解。我们在含有血红素和 NaCl 的实验室培养基中培养表皮葡萄球菌生物膜,以稳定二级 DNA 结构,并通过免疫标记和荧光显微镜观察其位置。我们还通过光相干断层扫描观察宏观生物膜结构。我们开发了定量测定不同核酸酶对 Z-DNA 和 G-四链体 DNA 寡聚物降解的方法,然后研究了这些酶如何影响生物膜中的 eDNA。Z-DNA 和 G-四链体 DNA 在生物膜基质中丰富,并且经常存在于网状结构中。在体外,如果没有 NaCl 或在生物膜生长过程中机械摇动,或者在缺乏 eDNA 或胞外多糖产生的细菌菌株中,这些结构都不会形成。因此,我们推断 eDNA 和多糖相互作用,在机械应力下导致非典型 DNA 结构,同时通过盐稳定。我们还证实,在感染小鼠植入物相关骨髓炎模型中植入物相关感染的植入物生物膜中存在 G-四链体 DNA 和 Z-DNA。哺乳动物 DNase I 对 Z-DNA 和 G-四链体 DNA 没有活性,而微球菌核酸酶可以降解 G-四链体 DNA,而 S1 曲霉核酸酶可以降解 Z-DNA。微球菌核酸酶起源于金黄色葡萄球菌,因此可能是葡萄球菌生物膜分散的关键。除了其结构作用外,我们还首次表明,在血红素存在的情况下,生物膜中的 eDNA 形成具有过氧化物酶样活性的 DNA 酶。虽然过氧化物酶是宿主防御病原体的一部分,但我们现在表明,生物膜可以在细胞外基质中具有内在的过氧化物酶活性。