Long-Term Transcriptional Activity at Zero Growth of a Cosmopolitan Rare Biosphere Member
Long-Term Transcriptional Activity at Zero Growth of a Cosmopolitan Rare Biosphere Member
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DOI：
10.1128/mbio.02189-18
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发表时间：
2019-01-01
期刊：
影响因子：
6.4
通讯作者：
Pester, Michael
中科院分区：
文献类型：
--
作者：
Hausmann, Bela;Pelikan, Claus;Pester, Michael
环境中的微生物多样性主要隐藏在稀有生物圈中(所有物种的相对丰度均为0.1%)。虽然休眠很好地解释了低丰度状态，但导致稀有但活跃的微生物的机制仍然难以捉摸。我们使用环境系统生物学来描述“Candidatus Desulfosporosinus frequens”的基因组和转录特征，这是一种从淡水湿地到淡水湿地的低丰度硫酸盐还原微生物，在那里它有助于神秘的硫循环。我们通过酸性泥炭土壤的超基因组学方法获得了它的近全基因组。此外，我们还利用Desulfosporosinus靶标的qPCR和转录组学技术对模拟原位培养50天的缺氧泥炭土进行了分析。在所有培养条件下，Desulfosporinus种群一直保持较低的丰度，平均每厘米土壤中16S rRNA基因拷贝数为1.2×10(6)。相反，与无底物对照相比，当提供少量的醋酸盐、丙酸盐、乳酸盐或丁酸盐修饰剂时，“少见德硫孢霉菌”的转录活性在第36天增加了56-188倍。总的转录活性是由编码核糖体蛋白、能量代谢和应激反应的基因驱动的，而不是由编码细胞生长相关过程的基因驱动的。由于我们的结果不支持这些高度活跃的微生物在生物量增加或细胞分裂方面的生长，它们不得不投入唯一的能量进行维护，很可能抵消了酸性pH条件。这一发现解释了一个稀有生物圈成员如何在50天内保持零增长状态的同时，对与生物地球化学相关的过程做出贡献。重要的是，微生物稀有生物圈代表着地球上最大的生物多样性池，总而言之，它的所有成员构成了栖息地生物量的相当大一部分。休眠或饥饿通常被用来解释低丰度微生物在环境中的持久性。我们表明，低丰度微生物可以在保持零增长状态至少7周的情况下具有高度转录活性。我们的结果提供了证据，证明在高细胞活动状态下的零增长是由维护要求驱动的。我们证明了这一点对于微生物Keystone物种来说是正确的，尤其是湿地中一种世界性的但永久低丰度的硫酸盐还原微生物，它参与了抵消温室气体排放。总之，我们的结果在理解与生态系统功能相关的稀有生物圈成员的时间分辨活动方面向前迈出了重要的一步。
Microbial diversity in the environment is mainly concealed within the rare biosphere (all species with < 0.1% relative abundance). While dormancy explains a low-abundance state very well, the mechanisms leading to rare but active microorganisms remain elusive. We used environmental systems biology to genomically and transcriptionally characterize "Candidatus Desulfosporosinus infrequens," a low-abundance sulfate-reducing microorganism cosmopolitan to freshwater wetlands, where it contributes to cryptic sulfur cycling. We obtained its near-complete genome by metagenomics of acidic peat soil. In addition, we analyzed anoxic peat soil incubated under in situ-like conditions for 50 days by Desulfosporosinus-targeted qPCR and metatranscriptomics. The Desulfosporosinus population stayed at a constant low abundance under all incubation conditions, averaging 1.2 x 10(6) 16S rRNA gene copies per cm (3) soil. In contrast, transcriptional activity of " Ca. Desulfosporosinus infrequens" increased at day 36 by 56- to 188-fold when minor amendments of acetate, propionate, lactate, or butyrate were provided with sulfate, compared to the no-substrate-control. Overall transcriptional activity was driven by expression of genes encoding ribosomal proteins, energy metabolism, and stress response but not by expression of genes encoding cell growth-associated processes. Since our results did not support growth of these highly active microorganisms in terms of biomass increase or cell division, they had to invest their sole energy for maintenance, most likely counterbalancing acidic pH conditions. This finding explains how a rare biosphere member can contribute to a biogeochemically relevant process while remaining in a zero-growth state over a period of 50 days.IMPORTANCE The microbial rare biosphere represents the largest pool of biodiversity on Earth and constitutes, in sum of all its members, a considerable part of a habitat's biomass. Dormancy or starvation is typically used to explain the persistence of low-abundance microorganisms in the environment. We show that a low-abundance microorganism can be highly transcriptionally active while remaining in a zero-growth state for at least 7 weeks. Our results provide evidence that this zero growth at a high cellular activity state is driven by maintenance requirements. We show that this is true for a microbial keystone species, in particular a cosmopolitan but permanently low-abundance sulfate-reducing microorganism in wetlands that is involved in counterbalancing greenhouse gas emissions. In summary, our results provide an important step forward in understanding time-resolved activities of rare biosphere members relevant for ecosystem functions.