金属供应影响生命早期微生物生态学和群落演替。

IF 5.1 1区 生物学 Q1 MICROBIOLOGY mBio Pub Date : 2024-11-13 Epub Date: 2024-10-23 DOI:10.1128/mbio.01534-24
Joshua Soto Ocaña, Elliot S Friedman, Orlaith Keenan, Nile U Bayard, Eileen Ford, Ceylan Tanes, Matthew J Munneke, William N Beavers, Eric P Skaar, Kyle Bittinger, Babette S Zemel, Gary D Wu, Joseph P Zackular
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引用次数: 0

摘要

肠道微生物群对人类的健康和疾病起着至关重要的作用。生命早期微生物群落的组合和演替受到多种因素的影响。反过来,已知这种微生物群落的集结会影响宿主,包括免疫系统的发育,并与以后的生活结果有关。迄今为止,还没有深入研究过宿主介导的营养免疫和金属可用性在形成生命早期微生物群落组合和演替中的作用。通过人类婴儿队列,我们发现金属螯合蛋白钙黏蛋白在婴儿中含量很高。以前被证明是婴儿肠道早期成功定殖者的类群,如肠球菌属、肠杆菌科和乳杆菌属,在培养过程中对实验性金属饥饿具有很强的抵抗力。而乳酸杆菌则极易受金属限制的影响,这表明宿主介导的金属限制可能是影响婴儿肠道早期定殖类群适应性的一种机制。我们进一步证明,与母乳喂养的婴儿相比,配方奶喂养的婴儿胃肠道中的金属含量明显更高。与母乳喂养婴儿相比,金属含量高的配方奶喂养婴儿的微生物群落与母乳喂养婴儿截然不同,其中肠球菌、肠杆菌和克雷伯氏菌含量较高,这些类群对高浓度金属的毒性作用具有更强的抵抗力。这些数据凸显了微生物群落组合的新模式,并表明营养免疫和膳食金属在塑造微生物群最早定殖事件中发挥着未被重视的作用。 重要意义生命早期是微生物定殖人体胃肠道的关键窗口期。令人惊讶的是,我们对婴儿成功定植的规则以及影响生命早期微生物定植者成功的因素仍然知之甚少。在这项研究中,我们发现金属的可用性是生命早期微生物群集结和演替的一个重要因素。我们的研究表明,源自宿主的金属螯合蛋白--钙保护蛋白在婴儿体内含量很高,成功的生命早期定殖者可以克服金属限制。我们进一步证明,喂养方式(母乳与配方奶)会明显影响肠道中的金属含量,从而可能影响微生物群落的演替。我们的研究表明,金属是生命早期生态学中一个以前未被探索的方面,它可能在婴儿微生物群的早期形成过程中发挥关键作用。
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Metal availability shapes early life microbial ecology and community succession.

The gut microbiota plays a critical role in human health and disease. Microbial community assembly and succession early in life are influenced by numerous factors. In turn, assembly of this microbial community is known to influence the host, including immune system development, and has been linked to outcomes later in life. To date, the role of host-mediated nutritional immunity and metal availability in shaping microbial community assembly and succession early in life has not been explored in depth. Using a human infant cohort, we show that the metal-chelating protein calprotectin is highly abundant in infants. Taxa previously shown to be successful early colonizers of the infant gut, such as Enterococcus, Enterobacteriaceae, and Bacteroides, are highly resistant to experimental metal starvation in culture. Lactobacillus, meanwhile, is highly susceptible to metal restriction, pointing to a possible mechanism by which host-mediated metal limitation shapes the fitness of early colonizing taxa in the infant gut. We further demonstrate that formula-fed infants harbor markedly higher levels of metals in their gastrointestinal tract compared to breastfed infants. Formula-fed infants with high levels of metals harbor distinct microbial communities compared to breastfed infants, with higher levels of Enterococcus, Enterobacter, and Klebsiella, taxa which show increased resistance to the toxic effects of high metal concentrations. These data highlight a new paradigm in microbial community assembly and suggest an unappreciated role for nutritional immunity and dietary metals in shaping the earliest colonization events of the microbiota.IMPORTANCEEarly life represents a critical window for microbial colonization of the human gastrointestinal tract. Surprisingly, we still know little about the rules that govern the successful colonization of infants and the factors that shape the success of early life microbial colonizers. In this study, we report that metal availability is an important factor in the assembly and succession of the early life microbiota. We show that the host-derived metal-chelating protein, calprotectin, is highly abundant in infants and successful early life colonizers can overcome metal restriction. We further demonstrate that feeding modality (breastmilk vs formula) markedly impacts metal levels in the gut, potentially influencing microbial community succession. Our work suggests that metals, a previously unexplored aspect of early life ecology, may play a critical role in shaping the early events of microbiota assembly in infants.

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来源期刊
mBio
mBio MICROBIOLOGY-
CiteScore
10.50
自引率
3.10%
发文量
762
审稿时长
1 months
期刊介绍: mBio® is ASM''s first broad-scope, online-only, open access journal. mBio offers streamlined review and publication of the best research in microbiology and allied fields.
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