Nitrogen fixation (NF) and phosphorus solubilization (PS) play a key role in maintaining the stability of mangrove ecosystems. In China, the invasion of Spartina alterniflora has brought a serious threat to the mangrove ecosystem. However, systematic research on NF and PS in mangrove sediments has not been conducted, and limited studies have focused on the response of NF and PS to S. alterniflora invasion, particularly at different sediment depths. In the present study, shotgun metagenomics and quantitative PCR were used to study the 0- to 100-cm sediment profile of the mangrove ecosystem in the Beibu Gulf of China. Results showed that the PS potential of mangrove sediments was primarily caused by enzymes encoded by phoA, phoD, ppx, ppa, and gcd genes. S. alterniflora changed environmental factors, such as total nitrogen, total phosphorus, and total organic carbon, and enhanced the potential of NF and PS in sediments. Moreover, most microorganisms involved in NF or PS (NFOPSMs) responded positively to the invasion of S. alterniflora. Cd, available iron, and salinity were the key environmental factors that affected the distribution of NF and PS genes (NFPSGs) and NFOPSMs. A strong coupling effect was observed between NF and PS in the mangrove ecosystem. S. alterniflora invasion enhanced the coupling of NF and PS and the interaction of microorganisms involved in NF and PS (NFAPSM), thereby promoting the turnover of NP and improving sediment quality. Finally, 108 metagenome-assembled genomes involved in NF or PS were reconstructed to further evaluate NFOPSMs. IMPORTANCE This study revealed the efficient nutrient cycling mechanism of mangroves. Positive coupling effects were observed in sediment quality, NF and PS processes, and NFOPSMs with the invasion of S. alterniflora. This research contributed to the understanding of the effects of S. alterniflora invasion on the subtropical mangrove ecosystem and provided theoretical guidance for mangrove protection, restoration, and soil management. Additionally, novel NFOPSMs provided a reference for the development of marine biological fertilizers.
Keywords: Spartina alterniflora; mangrove ecosystem; nitrogen fixation; phosphorus solubilization; shotgun metagenomics.