Our understanding of how the oral anaerobe Porphyromonas gingivalis can persist below the gum line, induce ecological changes, and promote polymicrobial infections remains limited. P. gingivalis has long been described as a highly proteolytic and asaccharolytic pathogen that utilizes protein substrates as the main source for energy production and proliferation. Here, we report that P. gingivalis displays a metabolic plasticity that enables the exploitation of non-proteinaceous substrates, specifically the monocarboxylates pyruvate and lactate, as well as human serum components, for colonization and biofilm formation. We show that anabolism of carbohydrates from pyruvate is powered by catabolism of amino acids. Concomitantly, the expression of fimbrial adhesion is upregulated, leading to the enhancement of biofilm formation, stimulation of multispecies biofilm development, and increase of colonization and invasion of the primary gingival epithelial cells by P. gingivalis. These studies provide the first glimpse into the metabolic plasticity of P. gingivalis and its adaptation to the nutritional condition of the host niche. Our findings support the model that in response to specific nutritional parameters, P. gingivalis has the potential to promote host colonization and development of a pathogenic community.

我们对口腔厌氧菌牙龈卟啉单胞菌如何持续存在于牙龈线以下、诱发生态变化和促进多种微生物感染的理解仍然有限。长期以来，牙龈卟啉单胞菌一直被描述为一种高度蛋白水解和无糖分解的病原体，它利用蛋白质底物作为能量产生和增殖的主要来源。在这里，我们报告P. gingivalis显示出一种代谢可塑性，可以利用非蛋白质底物，特别是单羧酸丙酮酸和乳酸，以及人血清成分，用于定植和生物膜形成。我们表明，来自丙酮酸的碳水化合物的合成代谢是由氨基酸的分解代谢提供动力的。同时，菌毛粘附的表达上调，导致生物膜形成增强，刺激多种生物膜发育，以及牙龈卟啉单胞菌对原代牙龈上皮细胞的定植和侵袭增加。这些研究首次展示了牙龈卟啉单胞菌的代谢可塑性及其对宿主生态位营养状况的适应。我们的研究结果支持模型，即响应特定的营养参数，P. gingivalis有可能促进宿主定植和致病群落的发展。