Department of Microbiology, Biomedicine Discovery Institute, Monash University, Clayton, VIC 3800, Australia.
School of Ecosystem and Forest Sciences, University of Melbourne, Richmond, VIC 3121, Australia.
Proc Natl Acad Sci U S A. 2021 Jul 27;118(30). doi: 10.1073/pnas.2102625118.
Organoheterotrophs are the dominant bacteria in most soils worldwide. While many of these bacteria can subsist on atmospheric hydrogen (H), levels of this gas are generally insufficient to sustain hydrogenotrophic growth. In contrast, bacteria residing within soil-derived termite mounds are exposed to high fluxes of H due to fermentative production within termite guts. Here, we show through community, metagenomic, and biogeochemical profiling that termite emissions select for a community dominated by diverse hydrogenotrophic Actinobacteriota and Dormibacterota. Based on metagenomic short reads and derived genomes, uptake hydrogenase and chemosynthetic RuBisCO genes were significantly enriched in mounds compared to surrounding soils. In situ and ex situ measurements confirmed that high- and low-affinity H-oxidizing bacteria were highly active in the mounds, such that they efficiently consumed all termite-derived H emissions and served as net sinks of atmospheric H Concordant findings were observed across the mounds of three different Australian termite species, with termite activity strongly predicting H oxidation rates ( = 0.82). Cell-specific power calculations confirmed the potential for hydrogenotrophic growth in the mounds with most termite activity. In contrast, while methane is produced at similar rates to H by termites, mounds contained few methanotrophs and were net sources of methane. Altogether, these findings provide further evidence of a highly responsive terrestrial sink for H but not methane and suggest H availability shapes composition and activity of microbial communities. They also reveal a unique arthropod-bacteria interaction dependent on H transfer between host-associated and free-living microbial communities.
有机异养菌是全球大多数土壤中占主导地位的细菌。虽然许多这类细菌可以利用大气中的氢气 (H)，但这种气体的水平通常不足以维持氢营养生长。相比之下，栖息在土壤衍生的白蚁丘内的细菌由于白蚁肠道内的发酵产生而暴露在高通量的 H 中。在这里，我们通过群落、宏基因组和生物地球化学分析表明，白蚁排放物选择了一个由多样化的氢营养性放线菌门和栖居菌门组成的群落。基于宏基因组短读序列和衍生基因组，与周围土壤相比，在白蚁丘中，氢摄取氢化酶和化能合成 RuBisCO 基因显著富集。原位和体外测量证实，高亲和性和低亲和性的 H 氧化细菌在白蚁丘中高度活跃，能够有效地消耗所有白蚁衍生的 H 排放物，并成为大气 H 的净汇。在三个不同的澳大利亚白蚁物种的白蚁丘中观察到了一致的发现，白蚁活动强烈预测 H 氧化速率（= 0.82）。细胞特异性功率计算证实了在白蚁丘中进行氢营养生长的潜力，而大多数白蚁活动存在。相比之下，虽然白蚁产生的甲烷与 H 的速率相似，但白蚁丘中含有很少的甲烷营养菌，并且是甲烷的净源。总的来说，这些发现进一步证明了 H 是一种高度响应的陆地汇，但不是甲烷，并且表明 H 的可用性塑造了微生物群落的组成和活性。它们还揭示了一种依赖于宿主相关和自由生活微生物群落之间 H 转移的独特节肢动物-细菌相互作用。
