Interkingdom assemblages in human saliva display group-level surface mobility and disease-promoting emergent functions.
Interkingdom assemblages in human saliva display group-level surface mobility and disease-promoting emergent functions.
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DOI：
10.1073/pnas.2209699119
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发表时间：
2022-10-11
影响因子：
11.1
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中科院分区：
文献类型：
--
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真菌和细菌形成多细胞生物膜，导致许多人类感染。这些独特的微生物如何在时空上协调致病功能仍未得到研究。利用多尺度实时显微镜和计算分析，我们研究了人类唾液中真菌和细菌相互作用的动力学以及它们在牙齿表面上的生物膜发展。我们发现了结构化的跨界域组合，显示出增强集体表面定植、生存和生长的紧急功能。进一步的分析揭示了一种意想不到的群体级别的表面移动性，在不断增长的同时，协调的“跳跃”和“行走”运动。这些移动的生长细胞群促进了这两个物种在表面上的快速空间传播，导致了更广泛的牙齿腐烂。我们的发现表明，多细胞跨王国组装像超生物一样，具有如果没有共组装就无法实现的功能。真菌和细菌经常进行复杂的相互作用，例如在人体内形成多细胞生物膜。关于跨王国生物膜如何启动和结合成更高级别的群落以及不同物种在生物膜形成期间执行哪些功能的知识仍然有限。我们在儿童龋齿疾病患者的唾液中发现了高度结构化排列的白色念珠菌(真菌)和变形链球菌(细菌)的自然状态组合。进一步的分析表明，菌群附着在真菌酵母、菌丝和胞外多糖的网络中，这些菌群作为一个预先组装的细胞群结合到表面。与单独的物种相比，跨王国组合显示出紧急的功能，包括增强表面定植和生长速度，更强的抗菌剂耐受性，以及更好的抗剪切力。值得注意的是，我们发现，跨王国的组合显示了一种独特的迁移空间移动性，使生物膜能够在表面上快速扩散，并导致增强的、更广泛的牙齿腐烂。利用突变体、物种的选择性失活和选择性基质去除，我们证明了增强的抗逆性和表面流动性来自于胞外聚合物基质，并且需要这两个物种在组装中的存在。当菌丝伸展并接触表面时，移动性由真菌丝状物引导，以“向前跳跃的运动”抬起集合。细菌细胞群在不断生长的同时，可以在这个移动单元上搭便车，立体地在表面扩散，并与其他组合融合，促进群落扩张。总而言之，我们的结果揭示了人类唾液中的一种跨界组装，它的行为像一个超有机体，具有致病的紧急功能，如果没有共同组装，这些功能是无法实现的。
Fungi and bacteria form multicellular biofilms causing many human infections. How such distinctive microbes act in concert spatiotemporally to coordinate disease-promoting functionality remains understudied. Using multiscale real-time microscopy and computational analysis, we investigate the dynamics of fungal and bacterial interactions in human saliva and their biofilm development on tooth surfaces. We discovered structured interkingdom assemblages displaying emergent functionalities to enhance collective surface colonization, survival, and growth. Further analyses revealed an unexpected group-level surface mobility with coordinated “leaping-like” and “walking-like” motions while continuously growing. These mobile groups of growing cells promote rapid spatial spreading of both species across surfaces, causing more extensive tooth decay. Our findings show multicellular interkingdom assemblages acting like supraorganisms with functionalities that cannot be achieved without coassembly. Fungi and bacteria often engage in complex interactions, such as the formation of multicellular biofilms within the human body. Knowledge about how interkingdom biofilms initiate and coalesce into higher-level communities and which functions the different species carry out during biofilm formation remain limited. We found native-state assemblages of Candida albicans (fungi) and Streptococcus mutans (bacteria) with highly structured arrangement in saliva from diseased patients with childhood tooth decay. Further analyses revealed that bacterial clusters are attached within a network of fungal yeasts, hyphae, and exopolysaccharides, which bind to surfaces as a preassembled cell group. The interkingdom assemblages exhibit emergent functions, including enhanced surface colonization and growth rate, stronger tolerance to antimicrobials, and improved shear resistance, compared to either species alone. Notably, we discovered that the interkingdom assemblages display a unique form of migratory spatial mobility that enables fast spreading of biofilms across surfaces and causes enhanced, more extensive tooth decay. Using mutants, selective inactivation of species, and selective matrix removal, we demonstrate that the enhanced stress resistance and surface mobility arise from the exopolymeric matrix and require the presence of both species in the assemblage. The mobility is directed by fungal filamentation as hyphae extend and contact the surface, lifting the assemblage with a “forward-leaping motion.” Bacterial cell clusters can “hitchhike” on this mobile unit while continuously growing, to spread across the surface three-dimensionally and merge with other assemblages, promoting community expansion. Together, our results reveal an interkingdom assemblage in human saliva that behaves like a supraorganism, with disease-causing emergent functionalities that cannot be achieved without coassembly.
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