The marine environmental microbiome mediates physiological outcomes in host nematodes.

IF 4.4 1区 生物学 Q1 BIOLOGY BMC Biology Pub Date : 2024-10-08 DOI:10.1186/s12915-024-02021-w
Yiming Xue, Yusu Xie, Xuwen Cao, Liusuo Zhang
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Abstract

Background: Nematodes are the most abundant metazoans in marine sediments, many of which are bacterivores; however, how habitat bacteria affect physiological outcomes in marine nematodes remains largely unknown.  RESULTS: Here, we used a Litoditis marina inbred line to assess how native bacteria modulate host nematode physiology. We characterized seasonal dynamic bacterial compositions in L. marina habitats and examined the impacts of 448 habitat bacteria isolates on L. marina development, then focused on HQbiome with 73 native bacteria, of which we generated 72 whole genomes sequences. Unexpectedly, we found that the effects of marine native bacteria on the development of L. marina and its terrestrial relative Caenorhabditis elegans were significantly positively correlated. Next, we reconstructed bacterial metabolic networks and identified several bacterial metabolic pathways positively correlated with L. marina development (e.g., ubiquinol and heme b biosynthesis), while pyridoxal 5'-phosphate biosynthesis pathway was negatively associated. Through single metabolite supplementation, we verified CoQ10, heme b, acetyl-CoA, and acetaldehyde promoted L. marina development, while vitamin B6 attenuated growth. Notably, we found that only four development correlated metabolic pathways were shared between L. marina and C. elegans. Furthermore, we identified two bacterial metabolic pathways correlated with L. marina lifespan, while a distinct one in C. elegans. Strikingly, we found that glycerol supplementation significantly extended L. marina but not C. elegans longevity. Moreover, we comparatively demonstrated the distinct gut microbiota characteristics and their effects on L. marina and C. elegans physiology.

Conclusions: Given that both bacteria and marine nematodes are dominant taxa in sedimentary ecosystems, the resource presented here will provide novel insights to identify mechanisms underpinning how habitat bacteria affect nematode biology in a more natural context. Our integrative approach will provide a microbe-nematodes framework for microbiome mediated effects on host animal fitness.

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海洋环境微生物群介导宿主线虫的生理结果。
背景:线虫是海洋沉积物中最丰富的后生动物,其中许多都是食菌者;然而,栖息地细菌如何影响海洋线虫的生理结果在很大程度上仍是未知数。 结果:在此,我们利用一个滨海烈氏线虫近交系来评估本地细菌如何调节宿主线虫的生理机能。我们描述了L. marina栖息地的季节性动态细菌组成,研究了448种栖息地细菌分离物对L. marina发育的影响,然后重点研究了73种本地细菌的HQbiome,并生成了其中72种细菌的全基因组序列。意想不到的是,我们发现海洋原生细菌对L. marina及其陆生亲缘动物秀丽隐杆线虫发育的影响呈显著正相关。接下来,我们重建了细菌代谢网络,并确定了几种与L. marina发育正相关的细菌代谢途径(如泛喹醇和血红素b的生物合成),而吡哆醛5'-磷酸的生物合成途径则与之负相关。通过补充单一代谢物,我们验证了 CoQ10、血红素 b、乙酰-CoA 和乙醛可促进藻类生长,而维生素 B6 则会抑制生长。值得注意的是,我们发现只有四种与生长发育相关的代谢途径是L. marina和C. elegans共有的。此外,我们还发现两条细菌代谢途径与游仆虫的寿命相关,而在秀丽隐杆线虫中则有一条不同的代谢途径。令人震惊的是,我们发现补充甘油能显著延长L. marina的寿命,而不是C. elegans的寿命。此外,我们还比较展示了不同的肠道微生物群特征及其对L. marina和C. elegans生理的影响:鉴于细菌和海洋线虫都是沉积生态系统中的优势类群,本文介绍的资源将提供新的见解,以确定在更自然的环境中,栖息地细菌如何影响线虫生物学的机制。我们的综合方法将提供一个微生物-线虫框架,以了解微生物组对宿主动物健康的介导效应。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
BMC Biology
BMC Biology 生物-生物学
CiteScore
7.80
自引率
1.90%
发文量
260
审稿时长
3 months
期刊介绍: BMC Biology is a broad scope journal covering all areas of biology. Our content includes research articles, new methods and tools. BMC Biology also publishes reviews, Q&A, and commentaries.
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