Moitinho-Silva Lucas, Díez-Vives Cristina, Batani Giampiero, Esteves Ana Is, Jahn Martin T, Thomas Torsten
Centre for Marine Bio-Innovation and School of Biological, Earth and Environmental Sciences, The University of New South Wales, Sydney, New South Wales, Australia.
Marine Microbiology, GEOMAR Helmholtz Centre for Ocean Research, Kiel, Germany.
ISME J. 2017 Jul;11(7):1651-1666. doi: 10.1038/ismej.2017.25. Epub 2017 Mar 24.
Despite an increased understanding of functions in sponge microbiomes, the interactions among the symbionts and between symbionts and host are not well characterized. Here we reconstructed the metabolic interactions within the sponge Cymbastela concentrica microbiome in the context of functional features of symbiotic diatoms and the host. Three genome bins (CcPhy, CcNi and CcThau) were recovered from metagenomic data of C. concentrica, belonging to the proteobacterial family Phyllobacteriaceae, the Nitrospira genus and the thaumarchaeal order Nitrosopumilales. Gene expression was estimated by mapping C. concentrica metatranscriptomic reads. Our analyses indicated that CcPhy is heterotrophic, while CcNi and CcThau are chemolithoautotrophs. CcPhy expressed many transporters for the acquisition of dissolved organic compounds, likely available through the sponge's filtration activity and symbiotic carbon fixation. Coupled nitrification by CcThau and CcNi was reconstructed, supported by the observed close proximity of the cells in fluorescence in situ hybridization. CcPhy facultative anaerobic respiration and assimilation by diatoms may consume the resulting nitrate. Transcriptional analysis of diatom and sponge functions indicated that these organisms are likely sources of organic compounds, for example, creatine/creatinine and dissolved organic carbon, for other members of the symbiosis. Our results suggest that organic nitrogen compounds, for example, creatine, creatinine, urea and cyanate, fuel the nitrogen cycle within the sponge. This study provides an unprecedented view of the metabolic interactions within sponge-microbe symbiosis, bridging the gap between cell- and community-level knowledge.
尽管人们对海绵微生物群的功能有了更多了解，但共生体之间以及共生体与宿主之间的相互作用仍未得到充分表征。在此，我们在共生硅藻和宿主的功能特征背景下，重建了海绵同心柱星海绵微生物群内的代谢相互作用。从同心柱星海绵的宏基因组数据中获得了三个基因组 bins（CcPhy、CcNi 和 CcThau），它们分别属于变形菌门叶杆菌科、硝化螺旋菌属和奇古菌门亚硝化侏儒菌目。通过对同心柱星海绵宏转录组读数进行映射来估计基因表达。我们的分析表明，CcPhy 是异养型，而 CcNi 和 CcThau 是化能自养型。CcPhy 表达了许多用于获取溶解有机化合物的转运蛋白，这些化合物可能通过海绵的过滤活动和共生碳固定获得。通过荧光原位杂交观察到细胞紧密相邻，支持了 CcThau 和 CcNi 之间的耦合硝化作用。CcPhy 的兼性厌氧呼吸和硅藻的同化作用可能会消耗产生的硝酸盐。对硅藻和海绵功能的转录分析表明，这些生物可能是共生体其他成员有机化合物的来源，例如肌酸/肌酐和溶解有机碳。我们的结果表明，有机氮化合物，例如肌酸、肌酐、尿素和氰酸盐，为海绵内的氮循环提供了燃料。这项研究提供了海绵 - 微生物共生体内代谢相互作用的前所未有的观点，弥合了细胞水平和群落水平知识之间的差距。
