Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory

Discovery of chemoautotrophic symbiosis in the giant shipworm Kuphus polythalamia (Bivalvia: Teredinidae) extends wooden-steps theory
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DOI:
10.1073/pnas.1620470114
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发表时间:
2017-05-02
影响因子:
11.1
通讯作者:
Haygood, Margo G.
Haygood, Margo G.
中科院分区:
综合性期刊1区
文献类型:
--
作者:
Distel, Daniel L.;Altamia, Marvin A.;Haygood, Margo G.

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“木台阶”假说[Distel Dl,et al.(2000)自然403:725-726]提出,在深海热液喷口发现的大型化学合成贻贝是与沉没的木材和其他有机沉积物有关的小得多的物种的后代,这些祖先的内生共生体利用来自生物来源(例如腐烂的木材)的硫化氢,而不是来自喷口流体。在这里,我们表明,木材不仅是栖息地之间的垫脚石,也是巨型泥钻双壳贝类多发性海龟异养和化学自养共生的桥梁。这种稀有而神秘的物种在现存的双壳类中达到了最长的长度,是唯一被描述的在海洋沉积物而不是木材中挖洞的钻木科双壳类(船虫)的成员。我们的研究结果表明,该虫体内含有硫氧化的化学自养(硫代自养)细菌,而不是能分解纤维的共生体,而这种共生体允许其他船虫物种以木材为食物。它的共生体特征、在Teredinidae中的系统发育地位、与其他家族成员相比消化系统的退化以及与木材消化相关的形态特征的丧失表明,K.Polythalamia是一种化学自养型双壳类,是木食性(木质营养)祖先的后代。这是一个例子,其中化学自养内共生产生的置换祖先异养共生和报告纯培养硫代自养内共生菌。
The "wooden-steps" hypothesis [Distel DL, et al. (2000) Nature 403: 725-726] proposed that large chemosynthetic mussels found at deep-sea hydrothermal vents descend from much smaller species associated with sunken wood and other organic deposits, and that the endosymbionts of these progenitors made use of hydrogen sulfide from biogenic sources (e.g., decaying wood) rather than from vent fluids. Here, we show that wood has served not only as a stepping stone between habitats but also as a bridge between heterotrophic and chemoautotrophic symbiosis for the giant mud-boring bivalve Kuphus polythalamia. This rare and enigmatic species, which achieves the greatest length of any extant bivalve, is the only described member of the wood-boring bivalve family Teredinidae (shipworms) that burrows in marine sediments rather than wood. We show that K. polythalamia harbors sulfur-oxidizing chemoautotrophic (thioautotrophic) bacteria instead of the cellulolytic symbionts that allow other shipworm species to consume wood as food. The characteristics of its symbionts, its phylogenetic position within Teredinidae, the reduction of its digestive system by comparison with other family members, and the loss of morphological features associated with wood digestion indicate that K. polythalamia is a chemoautotrophic bivalve descended from wood-feeding (xylotrophic) ancestors. This is an example in which a chemoautotrophic endosymbiosis arose by displacement of an ancestral heterotrophic symbiosis and a report of pure culture of a thioautotrophic endosymbiont.