Department of Medical Microbiology and Immunology, School of Medicine and Public Health, University of Wisconsin, Madison, Wisconsin, USA.
Department of Bacteriology, College of Agricultural and Life Sciences, University of Wisconsin, Madison, Wisconsin, USA.
mSystems. 2022 Oct 26;7(5):e0067722. doi: 10.1128/msystems.00677-22. Epub 2022 Aug 15.
The skin microbiome is a key player in human health, with diverse functions ranging from defense against pathogens to education of the immune system. While recent studies have begun to shed light on the valuable role that skin microorganisms have in maintaining the skin barrier, a detailed understanding of the complex interactions that shape healthy skin microbial communities is limited. Cobamides, the vitamin B class of cofactor, are essential for organisms across the tree of life. Because this vitamin is only produced by a limited fraction of prokaryotes, cobamide sharing is predicted to mediate community dynamics within microbial communities. Here, we provide the first large-scale metagenomic assessment of cobamide biosynthesis and utilization in the skin microbiome. We show that while numerous and diverse taxa across the major bacterial phyla on the skin encode cobamide-dependent enzymes, relatively few species encode cobamide biosynthesis. We show that cobamide producers and users are integrated into the network structure of microbial communities across the different microenvironments of the skin and that changes in microbiome community structure and diversity are associated with the abundance of cobamide producers in the genus, for both healthy and diseased skin states. Finally, we find that cobamide biosynthesis is enriched only in species associated with hosts, including those prevalent on human skin. We confirm that the cofactor is produced in excess through quantification of cobamide production by human skin-associated species isolated in the laboratory. Taken together, our results reveal the potential for cobamide sharing within skin microbial communities, which we hypothesize mediates microbiome community dynamics and host interactions. The skin microbiome is essential for maintaining skin health and function. However, the microbial interactions that dictate microbiome structure, stability, and function are not well understood. Here, we investigate the biosynthesis and use of cobamides, a cofactor needed by many organisms but only produced by select prokaryotes, within the human skin microbiome. We found that while a large proportion of skin taxa encode cobamide-dependent enzymes, only a select few encode cobamide biosynthesis. Further, the abundance of cobamide-producing species is associated with skin microbiome diversity and structure, and within this genus, biosynthesis is enriched in host-associated species compared to environment-associated species. These findings identify cobamides as a potential mediator of skin microbiome dynamics and skin health.
皮肤微生物组是人类健康的关键因素，具有多种功能，包括抵御病原体和免疫系统教育等。尽管最近的研究已经开始揭示皮肤微生物在维持皮肤屏障方面的重要作用，但对于塑造健康皮肤微生物群落的复杂相互作用的详细理解是有限的。钴胺素是维生素 B 类辅因子，对生命之树中的所有生物都是必不可少的。由于这种维生素仅由有限数量的原核生物产生，因此预测钴胺素的共享会介导微生物群落中的群落动态。在这里，我们提供了对皮肤微生物组中钴胺素生物合成和利用的首次大规模宏基因组评估。我们表明，虽然皮肤主要细菌门的众多和多样的类群都编码依赖钴胺素的酶，但相对较少的物种编码钴胺素生物合成。我们表明，钴胺素生产者和使用者被整合到皮肤不同微环境中微生物群落的网络结构中，并且微生物群落结构和多样性的变化与属中钴胺素生产者的丰度相关，无论是健康还是患病的皮肤状态。最后，我们发现只有与宿主相关的物种中富含钴胺素生物合成，包括那些在人类皮肤上流行的物种。我们通过定量检测从实验室分离的与人类皮肤相关的物种的钴胺素产生来证实该辅因子是通过过量产生的。总之，我们的研究结果揭示了皮肤微生物群落中钴胺素共享的潜力，我们假设这种共享介导了微生物群落动态和宿主相互作用。皮肤微生物组对于维持皮肤健康和功能至关重要。然而，决定微生物组结构、稳定性和功能的微生物相互作用尚不清楚。在这里，我们研究了钴胺素的生物合成和利用，钴胺素是许多生物体所需的辅因子，但仅由少数原核生物产生，在人类皮肤微生物组中。我们发现，虽然很大一部分皮肤类群编码依赖钴胺素的酶，但只有少数几个类群编码钴胺素生物合成。此外，产生钴胺素的物种的丰度与皮肤微生物组的多样性和结构相关，并且在这个属中，与环境相关的物种相比，宿主相关的物种中 生物合成更为丰富。这些发现将钴胺素确定为皮肤微生物组动态和皮肤健康的潜在介质。
