School of Ecological and Environmental Sciences, East China Normal University, Shanghai, China.
State Key Laboratory of Nutrient Use and Management, College of Resources and Environmental Sciences, Key Laboratory of Plant-Soil Interactions, National Academy of Agriculture Green Development, China Agricultural University, Beijing, China.
Microbiome. 2024 Nov 14;12(1):238. doi: 10.1186/s40168-024-01952-4.
Arsenic (As) metabolism pathways and their coupling to nitrogen (N) and carbon (C) cycling contribute to elemental biogeochemical cycling. However, how whole-microbial communities respond to As stress and which taxa are the predominant As-transforming bacteria or archaea in situ remains unclear. Hence, by constructing and applying ROCker profiles to precisely detect and quantify As oxidation (aioA, arxA) and reduction (arrA, arsC1, arsC2) genes in short-read metagenomic and metatranscriptomic datasets, we investigated the dominant microbial communities involved in arsenite (As(III)) oxidation and arsenate (As(V)) reduction and revealed their potential pathways for coupling As with N and C in situ in rice paddies.
Five ROCker models were constructed to quantify the abundance and transcriptional activity of short-read sequences encoding As oxidation (aioA and arxA) and reduction (arrA, arsC1, arsC2) genes in paddy soils. Our results revealed that the sub-communities carrying the aioA and arsC2 genes were predominantly responsible for As(III) oxidation and As(V) reduction, respectively. Moreover, a newly identified As(III) oxidation gene, arxA, was detected in genomes assigned to various phyla and showed significantly increased transcriptional activity with increasing soil pH, indicating its important role in As(III) oxidation in alkaline soils. The significant correlation of the transcriptional activities of aioA with the narG and nirK denitrification genes, of arxA with the napA and nirS denitrification genes and of arrA/arsC2 with the pmoA and mcrA genes implied the coupling of As(III) oxidation with denitrification and As(V) reduction with methane oxidation. Various microbial taxa including Burkholderiales, Desulfatiglandales, and Hyphomicrobiales (formerly Rhizobiales) are involved in the coupling of As with N and C metabolism processes. Moreover, these correlated As and N/C genes often co-occur in the same genome and exhibit greater transcriptional activity in paddy soils with As contamination than in those without contamination.
Our results revealed the comprehensive detection and typing of short-read sequences associated with As oxidation and reduction genes via custom-built ROCker models, and shed light on the various microbial taxa involved in the coupling of As and N and C metabolism in situ in paddy soils. The contribution of the arxA sub-communities to the coupling of As(III) oxidation with nitrate reduction and the arsC sub-communities to the coupling of As(V) reduction with methane oxidation expands our knowledge of the interrelationships among As, N, and C cycling in paddy soils. Video Abstract.
砷（As）代谢途径及其与氮（N）和碳（C）循环的耦合作用促进了元素生物地球化学循环。然而，整个微生物群落如何应对砷胁迫，以及哪些分类群是原位主要的砷转化细菌或古菌，仍不清楚。因此，通过构建和应用 ROCker 谱来精确检测和定量短读宏基因组和宏转录组数据集中的砷氧化（aioA、arxA）和还原（arrA、arsC1、arsC2）基因，我们研究了参与亚砷酸盐（As(III))氧化和砷酸盐（As(V))还原的主要微生物群落，并揭示了它们在原位将砷与 N 和 C 耦合的潜在途径在稻田中。
构建了五个 ROCker 模型来定量编码砷氧化（aioA 和 arxA）和还原（arrA、arsC1、arsC2）基因的短读序列的丰度和转录活性在稻田土壤中。我们的结果表明，携带 aioA 和 arsC2 基因的亚群落主要负责 As(III)氧化和 As(V)还原。此外，在分配给不同门的基因组中检测到了一个新的砷（III）氧化基因 arxA，并随着土壤 pH 的增加而显示出显著增加的转录活性，表明其在碱性土壤中砷（III）氧化中的重要作用。aioA 的转录活性与narG 和 nirK 反硝化基因、arxA 的转录活性与 napA 和 nirS 反硝化基因以及 arrA/arsC2 的转录活性与 pmoA 和 mcrA 基因之间的显著相关性表明砷（III）氧化与反硝化和砷（V)还原与甲烷氧化相耦合。包括伯克霍尔德氏菌目、脱硫脂肪杆菌目和丝状菌目（以前的根瘤菌目）在内的各种微生物类群参与了砷与 N 和 C 代谢过程的耦合。此外，这些相关的 As 和 N/C 基因经常在同一基因组中共存，并在受 As 污染的稻田中表现出比未受污染的稻田更高的转录活性。
我们的研究结果通过定制的 ROCker 模型揭示了与砷氧化和还原基因相关的短读序列的综合检测和分型，并阐明了原位参与稻田中砷与 N 和 C 代谢耦合的各种微生物类群。亚群落 arxA 对砷（III）氧化与硝酸盐还原偶联的贡献，以及 arsC 亚群落对砷（V）还原与甲烷氧化偶联的贡献，扩展了我们对稻田中砷、N 和 C 循环相互关系的认识。视频摘要。
