Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola.

Adaptations to submarine hydrothermal environments exemplified by the genome of Nautilia profundicola.
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DOI:
10.1371/journal.pgen.1000362
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发表时间:
2009-02
期刊:
影响因子:
4.5
通讯作者:
Cary, S. Craig
Cary, S. Craig
中科院分区:
生物学2区
文献类型:
--
作者:
Campbell, Barbara J.;Smith, Julie L.;Hanson, Thomas E.;Klotz, Martin G.;Stein, Lisa Y.;Lee, Charles K.;Wu, Dongying;Robinson, Jeffrey M.;Khouri, Hoda M.;Eisen, Jonathan A.;Cary, S. Craig

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海底热液喷口是太古代地球环境的模型系统,一些地点保持着可能有利于细胞生命形成和演化的条件。通风口的典型特征是温度和氧化还原电位的快速波动,这对居住的微生物群落施加了强大的选择压力。深海鹦鹉螺菌株Am-H是一种中等嗜热性,深分支的Epsilonproteobacterium,发现于热液喷口自由生活,是喷口多毛纲(Alvinella pompejana)背表面微生物群的成员。对N. profundicola 1.7 mbp基因组的分析揭示了其对喷口环境的适应——一些是独特的,一些是与其他epsilonproteobacterium基因组共有的。主要发现包括:(1)多种氢化酶与相对简单的电子传递链耦合;(2)多种应激反应系统;(3)一种新的预测硝酸盐同化途径,羟胺作为关键中间体;(4)一种基因(rgy)编码超嗜热生长的标志蛋白,逆回酶。进一步的实验表明,菌株Am-H的rgy表达比该细菌的最佳生长温度高出20°C,诱导rgy表达超过100倍,并且在地理上不同的嗜热环境中存在密切相关的rgy基因,并在细菌群落中表达。因此,N. profundicola是一种典型的Epsilonproteobacterium,它包含了在极端条件下生命所必需的所有基因,人们普遍认为这种极端条件反映了太古生物圈的条件——厌氧、富含硫、H2和co2,具有波动的氧化还原电位和温度。此外,对于生活在以快速和频繁的温度波动为特征的生态位中的中温和中度嗜热生物来说,逆回酶似乎是一种重要和共同的适应,因此不能再被认为是超嗜热生物的独特特征。极端环境,如深海热液喷口,位于海洋表面以下2500米,通过微生物介导的碳固定过程,利用化学物质(化学自养)而不是光(光自养),支持大型动物群落。一种这样的模式化学自养微生物,N. profundicola,基因组测序和描述在这项工作。N. profundicola是致病性幽门螺杆菌和弯曲杆菌的远亲,含有许多在DNA修复、环境感知和代谢中重要的基因和途径,这些基因和途径对其分支或所有微生物都是新的。这些基因和推断的代谢途径包括几种氢吸收和释放系统以及一种新的预测的氮同化途径。一种参与DNA修复的基因,逆转录酶,被认为是超嗜热微生物的标志蛋白,这种微生物生长在80°C以上。我们发现该基因在65°C时高度表达,比该生物的最佳生长温度高出20°C以上。因此,这种深海热液喷口化学自养模式的基因组可能反映了极端环境下生命所需的条件,假设类似于早期地球条件。
Submarine hydrothermal vents are model systems for the Archaean Earth environment, and some sites maintain conditions that may have favored the formation and evolution of cellular life. Vents are typified by rapid fluctuations in temperature and redox potential that impose a strong selective pressure on resident microbial communities. Nautilia profundicola strain Am-H is a moderately thermophilic, deeply-branching Epsilonproteobacterium found free-living at hydrothermal vents and is a member of the microbial mass on the dorsal surface of vent polychaete, Alvinella pompejana. Analysis of the 1.7-Mbp genome of N. profundicola uncovered adaptations to the vent environment—some unique and some shared with other Epsilonproteobacterial genomes. The major findings included: (1) a diverse suite of hydrogenases coupled to a relatively simple electron transport chain, (2) numerous stress response systems, (3) a novel predicted nitrate assimilation pathway with hydroxylamine as a key intermediate, and (4) a gene (rgy) encoding the hallmark protein for hyperthermophilic growth, reverse gyrase. Additional experiments indicated that expression of rgy in strain Am-H was induced over 100-fold with a 20°C increase above the optimal growth temperature of this bacterium and that closely related rgy genes are present and expressed in bacterial communities residing in geographically distinct thermophilic environments. N. profundicola, therefore, is a model Epsilonproteobacterium that contains all the genes necessary for life in the extreme conditions widely believed to reflect those in the Archaean biosphere—anaerobic, sulfur, H2- and CO2-rich, with fluctuating redox potentials and temperatures. In addition, reverse gyrase appears to be an important and common adaptation for mesophiles and moderate thermophiles that inhabit ecological niches characterized by rapid and frequent temperature fluctuations and, as such, can no longer be considered a unique feature of hyperthermophiles. Extreme environments, such as deep-sea hydrothermal vents, found 2,500 meters below the ocean surface, support large macrofaunal communities via microbially mediated carbon fixation processes using chemicals (chemoautotrophy) rather than light (photoautotrophy). The genome of one such model chemoautotrophic microbe, N. profundicola, was sequenced and described in this work. N. profundicola, distantly related to the pathogenic Helicobacter and Campylobacter species, contains a number of genes and pathways predicted to be important in DNA repair, environmental sensing, and metabolism, which are novel to either its subdivision or to all microbes. The genes and deduced metabolic pathways include several hydrogen uptake and release systems as well as a novel predicted nitrogen assimilation pathway. One gene involved in DNA repair, reverse gyrase, was thought to be a hallmark protein in hyperthermophiles, which are microbes that grow above 80°C. We found this gene to be highly expressed at 65°C, over 20°C above the optimal growth temperature of this organism. Therefore, the genome of this model deep-sea hydrothermal vent chemoautotroph may reflect what is required for life in an extreme environment, hypothesized to be similar to early earth conditions.
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