Mangrove wetlands have an active carbon and nitrogen cycle which is driven by diverse microorganisms. In our previous studies, AOA were found to contribute the main nitrification activity of nitrogen cycle in surface sediments of Zhangjiang estuary mangrove. But which AOA harbor in situ and how mangrove-AOA survival in this periodically-anoxic habitat is not well known. In order to further explore the habitat specificity and environmental adaption of AOA from mangrove sediments in China, amoA gene amplicon and metagenomic sequencing were performed in this study. A total of 145 OTUs were obtained by amplicon sequencing of mangrove sediments in Fujian (FJ), Zhejiang (ZJ), Guangdong (GD) and Hainan (HN) provinces. Through α diversity analysis, it was found that AOA in mangrove sediments of HN had higher species richness, while AOA in mangrove sediments of ZJ and GD had higher species numbers, and AOA in mangrove sediments of GD had the highest community diversity. The results of hierarchical cluster, NMDS and PCoA analyses showed that the AOA community structure of mangrove sediments in four different areas formed different clusters, which reflects the habitat specificity of AOA community in different mangroves. Phylogenetic analysis of all OTU sequences revealed that almost all AOA groups except thermophilic and acidophilic groups exist in situ. NS-δ and NS-IS-1 (mangrove-specific) group were found in mangrove sediments of all four different regions. And NS-IS-1 group have higher abundance in mangrove sediments of FJ and GD. However, ZJ mangrove was dominated by marine AOA groups. Through CCA analysis, it was found that ammonium and salinity were the most important environmental factors shaping AOA community. The results of correlation analysis showed that the ammonium had a significant positive correlation with the mangrove-specific group and a significant negative correlation with the marine AOA groups. For sediment salinity, the opposite is true. Fortunately, 3 metagenome-assembled genomes (MAGs) of mangrove-specific group AOA with high quality were obtained in GD samples. Through phylogenetic, ANI and AAI analyses, a new mangrove-specific genus Candidatus Nitrosomangrovi was proposed and this group was surprisingly predicted to own anaerobic carbon fixation pathway (Dicarboxylate-hydroxybutyrate cycle, DHC) in addition to the conventional 3- hydroxypropionate/4-hydroxybutyrate cycle (HHC) and ability of hydrogen oxidation, which can explain why it thrvived and possibly have important contributions to carbon and nitrogen cycles in periodically-anoxic environments. And genes for actate utilization were found in the genomes of Candidatus Nitrosomangrovi indicating the potential mixotrophic lifestyle of this group.