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Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds [Earth, Atmospheric, and Planetary Sciences]
Proceedings of the National Academy of Sciences of the United States of America ( IF 9.4 ) Pub Date : 2021-07-27 , DOI: 10.1073/pnas.2102625118
Eleonora Chiri 1, 2 , Philipp A Nauer 3, 4 , Rachael Lappan 2 , Thanavit Jirapanjawat 1 , David W Waite 5, 6 , Kim M Handley 5 , Philip Hugenholtz 6 , Perran L M Cook 4 , Stefan K Arndt 2 , Chris Greening 7
Affiliation  

Organoheterotrophs are the dominant bacteria in most soils worldwide. While many of these bacteria can subsist on atmospheric hydrogen (H2), 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 H2 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 H2-oxidizing bacteria were highly active in the mounds, such that they efficiently consumed all termite-derived H2 emissions and served as net sinks of atmospheric H2. Concordant findings were observed across the mounds of three different Australian termite species, with termite activity strongly predicting H2 oxidation rates (R2 = 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 H2 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 H2 but not methane and suggest H2 availability shapes composition and activity of microbial communities. They also reveal a unique arthropod–bacteria interaction dependent on H2 transfer between host-associated and free-living microbial communities.



中文翻译:

白蚁丘中氢营养微生物群落的白蚁气体排放选择[地球、大气和行星科学]

有机异养菌是全世界大多数土壤中的主要细菌。虽然这些细菌中有许多可以依靠大气中的氢 (H 2 ) 生存,但这种气体的含量通常不足以维持氢营养的生长。相反,居住在源自土壤的白蚁丘中的细菌暴露于高通量的 H 2由于白蚁肠道内的发酵产生。在这里,我们通过群落、宏基因组和生物地球化学分析表明,白蚁排放选择了一个由多种氢营养放线菌门和睡杆菌门主导的群落。基于宏基因组短读长和衍生基因组,与周围土壤相比,土丘中吸收氢化酶和化学合成的 RuBisCO 基因显着富集。原位和异位测量证实,高亲和力和低亲和力的 H 2氧化细菌在土丘中具有高度活性,因此它们有效地消耗了所有白蚁衍生的 H 2排放物并充当大气 H 2的净汇. 在三种不同澳大利亚白蚁物种的土丘中观察到一致的发现,白蚁活动强烈预测 H 2氧化率 ( R 2 = 0.82)。细胞特异性功率计算证实了白蚁活动最多的土丘中氢营养生长的潜力。相比之下,虽然白蚁以与 H 2相似的速率产生甲烷,但土丘中含有很少的甲烷氧化菌,并且是甲烷的净来源。总之,这些发现提供了对 H 2而不是甲烷的高度响应的陆地汇的进一步证据,并表明 H 2可用性决定了微生物群落的组成和活动。他们还揭示了一种独特的节肢动物-细菌相互作用,这种相互作用依赖于宿主相关微生物群落和自由生活微生物群落之间的H 2转移。

更新日期:2021-07-21
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