Spartina alterniflora invasion drastically increases methane production potential by shifting methanogenesis from hydrogenotrophic to methylotrophic pathway in a coastal marsh

Abstract

Abstract Plant invasion can strongly influence carbon (C) cycling processes, thus it may affect climate change by altering C sequestration and greenhouse gas emissions in the invaded ecosystem. Since 1979, the exotic Spartina alterniflora has rapidly expanded in China’s coastal areas, where significant increase in methane (CH4) emissions has been documented from post‐invaded sites. However, a mechanistic understanding of the structural and functional changes of associated methanogens accompanying this invasion remains elusive. Here we conducted integrated biogeochemical investigations on methanogenic substrates, activity, and diversity to identify implications of S. alterniflora invasion for methanogenesis in coastal wetlands. To do this, we collected and analysed 0–50 cm soil profiles from an uncolonised tidal flat (TF) and salt marshes that S. alterniflora has invaded for 1 year (SA‐1) and 12 years (SA‐12) in Jiangsu, China. Methanogenic community composition was characterised by massive parallel sequencing. The rates and pathways of methanogenesis were determined by adding trace concentrations of 13C‐labelled substrates to anaerobic incubated samples. Our results revealed that 12‐year invasion of S. alterniflora drastically increased CH4 production potential by one order of magnitude over that of TF. This substantial increase was primarily attributed to methanogenesis from trimethylamine; its rates increased by two orders of magnitude over TF whereas those from acetate and H2/CO2 increased far less. Hydrogenotrophic methanogenesis was the dominant pathway operating in the TF, but methanotrophic pathway contributed most to CH4 production in the surface layer of SA‐1 and uppermost 40‐cm layers of SA‐12. Consistent with these observations, the dominant methanogens shifted from obligate hydrogenotrophic Methanococcales in TF to potential methylamine‐utilising Methanosarcinaceaein SA‐12. Our Mantel analysis indicated that ‘non‐competitive’ trimethylamine, derived from cytoplasmic osmolytes of S. alterniflora, was the major driver of this change in methanogenic community composition. Synthesis. Our results suggest that invasive Spartina alternifloraplants gradually facilitated the local dominance of methylotrophic Methanosarcinaceae by changing the key type of methanogenic substrate in coastal marshes. Shifts in methanogen communities and enhanced availability of trimethylamine elevated the rates and importance of methylotrophic methanogenesis, thereby markedly increasing CH4 production potential and emission rates in this type of ecosystem.