Loss of microbial functional diversity following Spartina alterniflora invasion reduces the potential of carbon sequestration and nitrogen removal in mangrove sediments—from a gene perspective

Abstract

Mangrove ecosystems play an important role in carbon (C) sequestration and nitrogen (N) removal. Although Spartina alterniflora has successively invaded native mangrove habitats during the preceding two decades, the effects of this invasion on the microbial functional potential involved in nutrient cycling remain unclear. In this study, metagenomic sequencing was used to investigate microbial C and N cycling in sediments derived from S. alterniflora and three native mangrove species (Kandelia obovata, Avicennia marina, and Aegiceras corniculatum). Greater differences in functional profiles of C and N cycling-related genes were observed between S. alterniflora and mangrove sediments than between different mangrove sediments. Functional diversity was lower in S. alterniflora sediments than in native mangrove sediments. The growth of Thaumarchaeota and Proteobacteria, was enhanced due to their resilience to diversity loss, while the growth of oligotrophs, such as Chloroflexi and Firmicutes, was inhibited in S. alterniflora sediments. Compared to mangrove sediments, the abundance of genes involved in C fixation and methane production was lower in S. alterniflora sediments. However, S. alterniflora significantly increased the gene abundance of pmo which controlled the oxidation process of CH4 to carbon dioxide. Additionally, genes involved in nitrification were enriched, whereas genes involved in N reduction processes, such as denitrification and dissimilatory nitrate reduction to ammonium, N immobilization, and N mineralization, were depleted in S. alterniflora sediments compared to mangrove sediments. Partial least squares regression models demonstrated that the decrease in soil organic C and increase in pH after S. alterniflora invasion induced the loss of microbial functional diversity, which was the main driver of changes in the abundances of genes involved in C and N cycling. Overall, our findings indicate that S. alterniflora invasion modifies the microbial functional profile of nutrient cycling in native mangrove ecosystems and potentially weakens the capacity of mangroves to sequester carbon and remove nitrogen.