Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use
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DOI:
10.1073/pnas.1121198109
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发表时间:
2012-05-08
影响因子:
11.1
通讯作者:
Dubilier, Nicole
Dubilier, Nicole
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Kleiner, Manuel;Wentrup, Cecilia;Dubilier, Nicole

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低营养和能量供应导致了许多克服这些限制的策略的演变,其中共生协会是一个关键机制。特别引人注目的是化学合成细菌和海洋动物之间的联系,这些海洋动物在深海等营养贫乏的环境中茁壮成长,因为共生体允许它们的宿主在无机能源和碳源(如硫化物和二氧化碳)上生长。值得注意的是,很少有人知道的生理策略,使化学合成共生体殖民贫营养环境。在这项研究中,我们使用元蛋白质组学和代谢组学来研究Olavius algarvensis,一种没有勇气的海洋蠕虫,及其细菌共生体之间的化学合成关联的代谢相互作用的复杂网络。我们提出了以前未描述的途径来应对能量和营养限制,其中一些可能在自由生活和共生细菌中广泛存在。这些途径包括(i)宿主废物乙酸、丙酸、琥珀酸和苹果酸的共生体同化途径;(ii)一氧化碳作为能源的潜在用途,一种以前不知道在海洋无脊椎动物共生体中发挥作用的底物;(iii)氢作为能源的潜在用途;(iv)高亲和力摄取转运蛋白的强表达;(iv)一氧化碳作为能源的潜在用途。和(v)在CO2固定和硫酸盐还原中尚未描述的节能步骤。高表达的蛋白质参与途径的能量和碳的吸收和保护,在O。algarvensis共生表明,其环境的贫营养性质在形成这些协会方面施加了强大的选择压力。
Low nutrient and energy availability has led to the evolution of numerous strategies for overcoming these limitations, of which symbiotic associations represent a key mechanism. Particularly striking are the associations between chemosynthetic bacteria and marine animals that thrive in nutrient-poor environments such as the deep sea because the symbionts allow their hosts to grow on inorganic energy and carbon sources such as sulfide and CO2. Remarkably little is known about the physiological strategies that enable chemosynthetic symbioses to colonize oligotrophic environments. In this study, we used metaproteomics and metabolomics to investigate the intricate network of metabolic interactions in the chemosynthetic association between Olavius algarvensis, a gutless marine worm, and its bacterial symbionts. We propose previously undescribed pathways for coping with energy and nutrient limitation, some of which may be widespread in both free-living and symbiotic bacteria. These pathways include (i) a pathway for symbiont assimilation of the host waste products acetate, propionate, succinate and malate; (ii) the potential use of carbon monoxide as an energy source, a substrate previously not known to play a role in marine invertebrate symbioses; (iii) the potential use of hydrogen as an energy source; (iv) the strong expression of high-affinity uptake transporters; and (v) as yet undescribed energy-efficient steps in CO2 fixation and sulfate reduction. The high expression of proteins involved in pathways for energy and carbon uptake and conservation in the O. algarvensis symbiosis indicates that the oligotrophic nature of its environment exerted a strong selective pressure in shaping these associations.