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A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes.
Microbiome ( IF 15.5 ) Pub Date : 2020-06-23 , DOI: 10.1186/s40168-020-00877-y
Sheila Podell 1 , Jessica M Blanton 1 , Aaron Oliver 1 , Michelle A Schorn 2 , Vinayak Agarwal 3 , Jason S Biggs 4 , Bradley S Moore 5, 6, 7 , Eric E Allen 1, 5, 7, 8
Affiliation  

Marine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate organic matter. Lamellodysidea herbacea sponges obtain additional energy from abundant photosynthetic Hormoscilla cyanobacterial symbionts, which also produce polybrominated diphenyl ethers (PBDEs) chemically similar to anthropogenic pollutants of environmental concern. Potential contributions of non-Hormoscilla bacteria to Lamellodysidea microbiome metabolism and the synthesis and degradation of additional secondary metabolites are currently unknown. This study has determined relative abundance, taxonomic novelty, metabolic capacities, and secondary metabolite potential in 21 previously uncharacterized, uncultured Lamellodysidea-associated microbial populations by reconstructing near-complete metagenome-assembled genomes (MAGs) to complement 16S rRNA gene amplicon studies. Microbial community compositions aligned with sponge host subgroup phylogeny in 16 samples from four host clades collected from multiple sites in Guam over a 3-year period, including representatives of Alphaproteobacteria, Gammaproteobacteria, Oligoflexia, and Bacteroidetes as well as Cyanobacteria (Hormoscilla). Unexpectedly, microbiomes from one host clade also included Cyanobacteria from the prolific secondary metabolite-producer genus Prochloron, a common tunicate symbiont. Two novel Alphaproteobacteria MAGs encoded pathways diagnostic for methylotrophic metabolism as well as type III secretion systems, and have been provisionally assigned to a new order, designated Candidatus Methylospongiales. MAGs from other taxonomic groups encoded light-driven energy production pathways using not only chlorophyll, but also bacteriochlorophyll and proteorhodopsin. Diverse heterotrophic capabilities favoring aerobic versus anaerobic conditions included pathways for degrading chitin, eukaryotic extracellular matrix polymers, phosphonates, dimethylsulfoniopropionate, trimethylamine, and benzoate. Genetic evidence identified an aerobic catabolic pathway for halogenated aromatics that may enable endogenous PBDEs to be used as a carbon and energy source. The reconstruction of high-quality MAGs from all microbial taxa comprising greater than 0.1% of the sponge microbiome enabled species-specific assignment of unique metabolic features that could not have been predicted from taxonomic data alone. This information will promote more representative models of marine invertebrate microbiome contributions to host bioenergetics, the identification of potential new sponge parasites and pathogens based on conserved metabolic and physiological markers, and a better understanding of biosynthetic and degradative pathways for secondary metabolites and halogenated compounds in sponge-associated microbiota.

中文翻译:

进化枝特定Lamellodysidea海绵微生物群中营养和代谢多样性的基因组视图。

海洋海绵及其微生物群落对全球珊瑚礁中的碳和养分循环,加工和再矿化溶解的和颗粒状的有机物质做出了重要贡献。Lamellodysidea除草剂海绵从丰富的光合Hormoscilla蓝细菌共生体中获得更多能量,该共生体还产生多溴化二苯醚(PBDEs),其化学性质与人为污染的环境相似。目前尚不知道非大肠菌对Lamellodysidea微生物组代谢以及其他次级代谢产物的合成和降解的潜在贡献。这项研究确定了21个以前未表征的相对丰度,分类学上的新颖性,代谢能力和次生代谢产物的潜力,重构近乎完整的基因组组装基因组(MAGs),以补充16S rRNA基因扩增子研究,从而培养未培养的Lamellodysidea相关微生物种群。在三年的时间里,从关岛多个地点收集的四个宿主进化枝中的16个样品中,与海绵宿主亚群系统发育相一致的微生物群落组成,包括Alphaproteobacteria,Gammaproteobacteria,Oligoflexia和Bacteroidetes以及Cyanobacteria(Hormoscilla)的代表。出乎意料的是,来自一个宿主进化枝的微生物群也包括来自多产次生代谢产物产生者Prochloron属的蓝藻,这是一种常见的被膜生物。两个新的Alteproteobacteria MAGs编码了诊断甲基营养型代谢以及III型分泌系统的途径,并已临时分配给新的订单,指定为念珠菌甲基海绵体。来自其他分类学组的MAG不仅使用叶绿素,而且还使用细菌叶绿素和蛋白视紫红质编码光驱动的能量产生途径。有利于有氧和厌氧条件的多种异养能力包括降解几丁质,真核细胞外基质聚合物,膦酸酯,二甲基磺基丙酸,三甲胺和苯甲酸酯的途径。遗传证据确定卤代芳烃的好氧分解代谢途径可能使内源性多溴二苯醚用作碳和能源。从占海绵微生物组0.1%以上的所有微生物类群中重建高质量MAG,可实现独特的代谢特征的物种特异性分配,这是仅凭分类学数据无法预测的。
更新日期:2020-06-23
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