Abstract:
Dimethylsulfoniopropionate (DMSP) and related organic sulfur compounds play key roles in global sulfur cycling. Bacteria have been found to be important DMSP producers in seawater and surface sediments of the aphotic Mariana Trench (MT). However, detailed bacterial DMSP cycling in the Mariana Trench subseafloor remains largely unknown. Here, the bacterial DMSP-cycling potential in a Mariana Trench sediment core (7.5 m in length) obtained at a 10,816-m water depth was investigated using culture-dependent and -independent methods. The DMSP content fluctuated along the sediment depth and reached the highest concentration at 15 to 18 cm below the seafloor (cmbsf). dsyB was the dominant known DMSP synthetic gene, existing in 0.36 to 1.19% of the bacteria, and was identified in the metagenome-assembled genomes (MAGs) of previously unknown bacterial DMSP synthetic groups such as Acidimicrobiia, Phycisphaerae, and Hydrogenedentia. dddP, dmdA, and dddX were the major DMSP catabolic genes. The DMSP catabolic activities of DddP and DddX retrieved from Anaerolineales MAGs were confirmed by heterologous expression, indicating that such anaerobic bacteria might participate in DMSP catabolism. Moreover, genes involved in methanethiol (MeSH) production from methylmercaptopropionate (MMPA) and dimethyl sulfide (DMS), MeSH oxidation, and DMS production were highly abundant, suggesting active conversions between different organic sulfur compounds. Finally, most culturable DMSP synthetic and catabolic isolates possessed no known DMSP synthetic and catabolic genes, and actinomycetes could be important groups involved in both DMSP synthesis and catabolism in Mariana Trench sediment. This study extends the current understanding of DMSP cycling in Mariana Trench sediment and highlights the need to uncover novel DMSP metabolic genes/pathways in extreme environments. IMPORTANCE Dimethylsulfoniopropionate (DMSP) is an abundant organosulfur molecule in the ocean and is the precursor for the climate-active volatile gas dimethyl sulfide. Previous studies focused mainly on bacterial DMSP cycling in seawater, coastal sediment, and surface trench sediment samples, but DMSP metabolism in the Mariana Trench (MT) subseafloor sediments remains unknown. Here, we describe the DMSP content and metabolic bacterial groups in the subseafloor of the MT sediment. We found that the tendency for vertical variation of the DMSP content in the MT was distinct from that of the continent shelf sediment. Although dsyB and dddP were the dominant DMSP synthetic and catabolic genes in the MT sediment, respectively, both metagenomic and culture methods revealed multiple previously unknown DMSP metabolic bacterial groups, especially anaerobic bacteria and actinomycetes. The active conversion of DMSP, DMS, and methanethiol may also occur in the MT sediments. These results provide novel insights for understanding DMSP cycling in the MT.
摘要:
二甲基磺丙酸酯(DMSP)和相关有机硫化合物在全球硫循环中起着关键作用。已发现细菌是无头马里亚纳海沟(MT)的海水和表面沉积物中重要的DMSP生产者。然而,在马里亚纳海沟海底的详细细菌DMSP循环仍然未知。这里,使用依赖于培养和独立的方法研究了在10,816-m水深处获得的马里亚纳海沟沉积物核心(长度为7.5m)中的细菌DMSP循环潜力。DMSP含量沿沉积物深度波动,并在海底以下15至18厘米(cmbsf)达到最高浓度。dsyB是已知的显性DMSP合成基因,存在于0.36至1.19%的细菌中,并在先前未知的细菌DMSP合成组的宏基因组组装基因组(MAG)中鉴定,例如酸性微生物,Phycisphaerae,和氢化痴呆。dddP,dmdA,和dddX是主要的DMSP分解代谢基因。通过异源表达证实了从AnaerolinealMAG中检索到的DddP和DddX的DMSP分解代谢活性,表明此类厌氧菌可能参与DMSP分解代谢。此外,涉及从甲基巯基丙酸酯(MMPA)和二甲基硫醚(DMS)生产甲硫醇(MeSH)的基因,MeSH氧化,DMS生产非常丰富,表明不同有机硫化合物之间的活性转化。最后,大多数可培养的DMSP合成和分解代谢分离株没有已知的DMSP合成和分解代谢基因,放线菌可能是马里亚纳海沟沉积物中DMSP合成和分解代谢的重要类群。这项研究扩展了目前对马里亚纳海沟沉积物中DMSP循环的理解,并强调了在极端环境中发现新型DMSP代谢基因/途径的必要性。重要性二甲基磺丙酸酯(DMSP)是海洋中丰富的有机硫分子,是气候活跃的挥发性气体二甲基硫醚的前体。以前的研究主要集中在海水中的细菌DMSP循环,沿海沉积物,和地表沟槽沉积物样本,但是马里亚纳海沟(MT)海底沉积物中的DMSP代谢仍然未知。这里,我们描述了MT沉积物海底的DMSP含量和代谢细菌群。我们发现,MT中DMSP含量的垂直变化趋势与大陆架沉积物不同。尽管dsyB和dddP是MT沉积物中主要的DMSP合成和分解代谢基因,分别,宏基因组和培养方法都揭示了多个以前未知的DMSP代谢细菌组,尤其是厌氧细菌和放线菌。DMSP的主动转换,DMS,甲硫醇也可能存在于MT沉积物中。这些结果为理解MT中的DMSP循环提供了新的见解。