Evidences of aromatic degradation dominantly via the phenylacetic acid pathway in marine benthic Thermoprofundales
Evidences of aromatic degradation dominantly via the phenylacetic acid pathway in marine benthic Thermoprofundales
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海洋底栖 Thermoprofundales 中芳香族化合物降解主要通过苯乙酸途径的证据
DOI：
10.1111/1462-2920.14850
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发表时间：
2020-01-01
影响因子：
5.1
通讯作者：
Zhou, Ning-Yi
中科院分区：
文献类型：
--
作者：
Liu, Wei-Wei;Pan, Jie;Zhou, Ning-Yi
Thermoprofundales（Marine Benthic Group D archaea，MBG-D）是一个新提出的古细菌目，广泛分布于全球海洋沉积物中，其成员可能在碳循环中发挥重要作用。然而，缺乏这些有机体的纯文化阻碍了他们的分解代谢作用的认识。本文通过构建热液沉积物中两个新亚群的高质量宏基因组组装基因组（MAGs），并预测其分解代谢途径，为热液沉积物中的热深藻能够通过苯乙酸（PAA）途径降解芳烃提供基因组证据。然后，在参考基因组中搜索PAA途径的关键酶苯乙酰辅酶A连接酶（PCL）的基因序列。PCL基因在14.9%的古生菌和75.9%的Thermoprofundales中的广泛分布进一步支持了PAA途径在古生菌中的重要性，特别是在没有发现环裂解双加氧酶的Thermoprofundales MAG中的两个PCL，PCLM 8 -3和PCLM 10 -15，能够在体外将PAA转化为苯乙酰辅酶A（PA-CoA），证明了Thermoprofundales经由CoA活化通过PAA参与芳烃降解。它们的耐酸性（pH 5-7）、高最适温度（60 ° C和80 ° C）、热稳定性（在60 ° C和50 ° C下稳定48小时）和宽底物谱意味着Thermoprofundales能够在极端条件下转化芳烃。与大多数相关的芳香族途径在Thermoprofundales基因的原位转录活性的证据，这些基因组和生化证据一起突出了这种无处不在的和丰富的古菌在海洋沉积物的碳循环中的重要作用。
Thermoprofundales (Marine Benthic Group D archaea, MBG-D) is a newly proposed archaeal order and widely distributed in global marine sediment, and the members in the order may play a vital role in carbon cycling. However, the lack of pure cultures of these oeganisms has hampered the recognition of their catabolic roles. Here, by constructing high-quality metagenome-assembled genomes (MAGs) of two new subgroups of Thermoprofundales from hydrothermal sediment and predicting their catabolic pathways, we here provide genomic evidences that Thermoprofundales are capable of degrading aromatics via the phenylacetic acid (PAA) pathway. Then, the gene sequences of phenylacetyl-CoA ligase (PCL), a key enzyme for the PAA pathway, were searched in reference genomes. The widespread distribution of PCL genes among 14.9% of archaea and 75.9% of Thermoprofundales further supports the importance of the PAA pathway in archaea, particularly in Thermoprofundales where no ring-cleavage dioxygenases were found. Two PCLs from Thermoprofundales MAGs, PCLM8-3 and PCLM10-15, were able to convert PAA to phenylacetyl-CoA (PA-CoA) in vitro, demonstrating the involvement of Thermoprofundales in aromatics degradation through PAA via CoA activation. Their acid tolerance (pH 5-7), high-optimum temperatures (60 degrees C and 80 degrees C), thermostability (stable at 60 degrees C and 50 degrees C for 48 h) and broad substrate spectra imply that Thermoprofundales are capable of transforming aromatics under extreme conditions. Together with the evidence of in situ transcriptional activities for most genes related to the aromatics pathway in Thermoprofundales, these genomic, and biochemical evidences highlight the essential role of this ubiquitous and abundant archaeal order in the carbon cycle of marine sediments.