Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean

Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean
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DOI:
10.1128/aem.71.9.5440-5450.2005
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发表时间:
2005-09-01
影响因子:
4.4
通讯作者:
Horikoshi, K
Horikoshi, K
中科院分区:
生物学2区
文献类型:
--
作者:
Suzuki, Y;Sasaki, T;Horikoshi, K

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这只来自印度中脊凯雷热液场的热液喷口腹足动物Alviniconcha affh . hessleri在其极大扩大的鳃内容纳了类似细菌的细胞。从鳃的DNA提取中获得了一个16S rRNA基因序列,系统发育分析将源生物置于变形菌门epsilon分支的谱系中。荧光原位杂交分析用寡核苷酸探针针对特定的epsilonproteobacteria亚群显示,细菌密集定植在鳃丝。无论腹足动物的细胞丰度如何,其组织部分的碳同位素均匀性表明,其生物量的碳同位素组成与腹足动物的大致相同。化合物特异性碳同位素分析表明,来自腹足动物组织的脂肪酸相对于腹足动物生物量都富含C-13,并且来自内共生生物的单不饱和C-16脂肪酸相对于腹足动物生物量的碳-13含量与在化学自养条件下生长的epsilonproteobacterial培养物的碳-13含量相同。这种分离模式很可能是由于基于还原性三羧酸(rTCA)循环和随后由富含c- 13的乙酰辅酶a合成的脂肪酸的化学自养。酶学表征显示rTCA循环的几个关键酶具有明显的活性,并且在鳃组织中缺乏核酮糖-1,5-二磷酸羧化酶/加氧酶活性。解剖学、分子系统发育、体积和化合物特异性碳同位素以及酶分析的结果都支持这样的推论,即来自印度洋的热液喷口腹足动物利用了一种依赖于epsilonproteobacteriendosymbiont的化学自养的新型营养策略。本研究的数据与先前关于太平洋Alviniconcha腹足类动物的数据之间的差异表明,至少有两个趋化自养细菌谱系,在细分水平上不同,作为一种宿主动物类型的主要内共生体出现。
The hydrothermal-vent gastropod Alviniconcha aff. hessleri from the Kairei hydrothermal field on the Central Indian Ridge houses bacterium-like cells internally in its greatly enlarged gill. A single 16S rRNA gene sequence was obtained from the DNA extract of the gill, and phylogenetic analysis placed the source organism within a lineage of the epsilon subdivision of the Proteobacteria. Fluorescence in situ hybridization analysis with an oligonucleotide probe targeting the specific epsilonproteobacterial subgroup showed the bacterium densely colonizing the gill filaments. Carbon isotopic homogeneity among the gastropod tissue parts, regardless of the abundance of the endosymbiont cells, suggests that the carbon isotopic composition of the endosymbiont biomass is approximately the same as that of the gastropod. Compound-specific carbon isotopic analysis revealed that fatty acids from the gastropod tissues are all C-13 enriched relative to the gastropod biomass and that the monounsaturated C-16 fatty acid that originates from the endosymbiont is as C-13 enriched relative to the gastropod biomass as that of the epsilonproteobacterial cultures grown under chemoautotrophic conditions. This fractionation pattern is most likely due to chemoautotrophy based on the reductive tricarboxylic-acid (rTCA) cycle and subsequent fatty acid biosynthesis from C-13-enriched acetyl coenzyme A. Enzymatic characterization revealed evident activity of several key enzymes of the rTCA cycle, as well as the absence of ribulose-1,5-bisphosphate carboxylase/oxygenase activity in the gill tissue. The results from anatomic, molecular phylogenetic, bulk and compound-specific carbon isotopic, and enzymatic analyses all support the inference that a novel nutritional strategy relying on chemoautotrophy in the epsilonproteobacterial endosymbiont is utilized by the hydrothermal-vent gastropod from the Indian Ocean. The discrepancies between the data of the present study and those of previous ones for Alviniconcha gastropods from the Pacific Ocean imply that at least two lineages of chemoautotrophic bacteria, phylogenetically distinct at the subdivision level, occur as the primary endosymbiont in one host animal type.