Division of labor and growth during electrical cooperation in multicellular cable bacteria

Division of labor and growth during electrical cooperation in multicellular cable bacteria
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DOI:
10.1073/pnas.1916244117
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发表时间:
2020-03-10
影响因子:
11.1
通讯作者:
Meysman, Filip J. R.
Meysman, Filip J. R.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Geerlings, Nicole M. J.;Karman, Cheryl;Meysman, Filip J. R.

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多细胞性是一个关键的进化创新,导致细胞之间的协调活动和资源共享,这通常通过化学物质的物理交换发生。然而,丝状电缆细菌显示出一种独特的代谢,其中远距离细胞的氧化还原转化是通过远距离电子传递而不是化学物质交换来耦合的。这挑战了我们对生物功能的理解,因为电缆细菌中电子传递、代谢、能量守恒和细丝生长之间的联系仍然是谜。在这里,我们发现电缆细菌的单个细丝内的细胞在生物合成中显示出显著的两分法,这与氧化还原带一致。纳米二级离子质谱结合C-13(碳酸氢盐和丙酸盐)和n -15-氨同位素标记表明,在较深的缺氧层中进行硫化物氧化的细胞具有较高的同化率,而在氧气区进行氧还原的细胞则很少或没有标签吸收。因此,氧还原似乎只是一种快速释放电子的机制,几乎没有能量守恒,而生物合成和生长仅限于硫化物呼吸细胞。尽管如此,当氧化还原条件发生变化时,细胞可以立即转换角色,而不表现出分化,这表明细胞在氧气区进行的“社区服务”只是暂时的。总的来说,我们的数据揭示了以前在多细胞生物中未见过的细胞之间的劳动分工和电合作。
Multicellularity is a key evolutionary innovation, leading to coordinated activity and resource sharing among cells, which generally occurs via the physical exchange of chemical compounds. However, filamentous cable bacteria display a unique metabolism in which redox transformations in distant cells are coupled via long-distance electron transport rather than an exchange of chemicals. This challenges our understanding of organismal functioning, as the link among electron transfer, metabolism, energy conservation, and filament growth in cable bacteria remains enigmatic. Here, we show that cells within individual filaments of cable bacteria display a remarkable dichotomy in biosynthesis that coincides with redox zonation. Nanoscale secondary ion mass spectrometry combined with C-13 (bicarbonate and propionate) and N-15-ammonia isotope labeling reveals that cells performing sulfide oxidation in deeper anoxic horizons have a high assimilation rate, whereas cells performing oxygen reduction in the oxic zone show very little or no label uptake. Accordingly, oxygen reduction appears to merely function as a mechanism to quickly dispense of electrons with little to no energy conservation, while biosynthesis and growth are restricted to sulfide-respiring cells. Still, cells can immediately switch roles when redox conditions change, and show no differentiation, which suggests that the "community service" performed by the cells in the oxic zone is only temporary. Overall, our data reveal a division of labor and electrical cooperation among cells that has not been seen previously in multicellular organisms.