A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes
A genomic view of trophic and metabolic diversity in clade-specific Lamellodysidea sponge microbiomes
复制标题
进化枝特异性板藻海绵微生物群落营养和代谢多样性的基因组学观点
DOI：
10.1186/s40168-020-00877-y
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发表时间：
2020-06-23
期刊：
影响因子：
15.5
通讯作者：
Allen, Eric E.
中科院分区：
文献类型：
--
作者：
Podell, Sheila;Blanton, Jessica M.;Allen, Eric E.
背景海洋海绵及其微生物组对全球珊瑚礁的碳和营养循环、溶解和颗粒有机物的加工和再矿化做出了重大贡献。 Lamellodysidea 草本海绵从丰富的光合荷尔莫西拉蓝细菌共生体中获得额外的能量，这些共生体也产生化学性质与环境问题的人为污染物类似的多溴二苯醚 (PBDE)。非激素颤菌对 Lamelodyside 微生物组代谢以及其他次级代谢物的合成和降解的潜在贡献目前尚不清楚。结果本研究通过重建近乎完整的宏基因组组装基因组 (MAG) 来补充 16S rRNA 基因扩增子研究，确定了 21 个先前未表征、未培养的 Lamellodysidea 相关微生物种群的相对丰度、分类新颖性、代谢能力和次级代谢潜力。在 3 年期间从关岛多个地点收集的 4 个宿主进化枝的 16 个样本中，微生物群落组成与海绵宿主亚群系统发育一致，其中包括 Alphaproteobacteria、Gammaproteobacteria、Oligoflexia、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组还包括来自多产的次生代谢产物原绿藻属的蓝藻，这是一种常见的被囊类共生体。两种新的 Alphaproteobacteria MAG 编码甲基营养代谢和 III 型分泌系统的诊断途径，并已暂时分配给一个新目，命名为 CandidatusMmethylospongiales。来自其他分类群的 MAG 不仅使用叶绿素，还使用细菌叶绿素和蛋白视紫红质编码光驱动的能量生产途径。有利于需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、膦酸盐、二甲基磺基丙酸盐、三甲胺和苯甲酸盐的途径。遗传证据确定了卤化芳香族化合物的有氧分解代谢途径，该途径可能使内源性多溴二苯醚能够用作碳和能源。结论 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，能够对独特的代谢特征进行物种特异性分配，而这些特征是仅从分类学数据无法预测的。这些信息将促进海洋无脊椎动物微生物组对宿主生物能学贡献的更具代表性的模型，基于保守的代谢和生理标记识别潜在的新海绵寄生虫和病原体，以及更好地了解海绵相关微生物群中次生代谢物和卤化化合物的生物合成和降解途径。
Background Marine sponges and their microbiomes contribute significantly to carbon and nutrient cycling in global reefs, processing and remineralizing dissolved and particulate organic matter.Lamellodysidea herbaceasponges obtain additional energy from abundant photosyntheticHormoscillacyanobacterial symbionts, which also produce polybrominated diphenyl ethers (PBDEs) chemically similar to anthropogenic pollutants of environmental concern. Potential contributions of non-Hormoscillabacteria toLamellodysideamicrobiome metabolism and the synthesis and degradation of additional secondary metabolites are currently unknown. Results This study has determined relative abundance, taxonomic novelty, metabolic capacities, and secondary metabolite potential in 21 previously uncharacterized, unculturedLamellodysidea-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 genusProchloron, 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, designatedCandidatusMethylospongiales. 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. Conclusions 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.