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Increasing Inundation Frequencies Enhance the Stochastic Process and Network Complexity of the Soil Archaeal Community in Coastal Wetlands.

ABSTRACT: Coastal wetlands are experiencing frequent flooding because of global climate changes, such as the rising sea level. Despite the key role of archaea in soil biogeochemical cycles, the assembly processes and co-occurrence patterns of archaeal communities in coastal wetlands in response to increasing inundation frequencies remain elusive. In this study, we established an in situ mesocosm with an inundation frequency gradient to investigate the response of soil archaeal community toward increasing inundation frequencies in monocultures of Spartina alterniflora and a mangrove species, Kandelia obovata Both neutral community model and null model analyses suggested that stochastic processes are dominant in governing the archaeal community assembly and that the stochastic processes are enhanced with increasing inundation frequencies. Increasing inundation frequencies significantly increased the community niche width. Moreover, archaeal community in S. alterniflora soil displayed lower niche overlap and higher stochasticity than in K. obovata soil. Co-occurrence network analysis revealed that the network complexity increases with increase in the inundation frequencies. Soil water content is the most decisive factor influencing the archaeal communities. Overall, we found that increasing inundation frequencies enhance the stochastic processes and network complexity of the soil archaeal community in coastal wetlands. This study could enhance our understanding on the response of soil archaeal communities in coastal wetlands toward global change.IMPORTANCE Coastal wetlands, subjected to regular disturbances by periodic tides, are highly productive and important in the regulation of climate change. However, the assembly mechanisms and co-occurrence patterns of soil archaeal communities in coastal areas remain poorly known, especially for their responses to increasing inundation frequencies. In this study, we aimed at unraveling these uncertainties by studying typical estuarine ecosystems in southern China. We show that increasing inundation frequencies enhance the stochastic processes and network complexity of the soil archaeal community. This study offers a new path for an improved understanding of archaeal community assembly and species coexistence in coastal environments, with a special focus on the role of inundation frequency.

SUBMITTER: Gao GF

PROVIDER: S-EPMC8208137 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Microbial communities commonly consist of a large number of rare taxa (RT) and few abundant taxa (AT), and it is important to identify the differences of the community assembly processes between RT and AT in response to environmental changes. However, the community assembly processes governing AT and RT in coastal wetland soils along an inundation gradient remain elusive. Here, an in situ mesocosm, with continuous inundation gradients and native mangrove Kandelia obovata or exotic cordgrass Spartina alterniflora, was established to determine the patterns and driving factors of community turnover and assembly processes of AT and RT. We found that RT exhibited a remarkably lower turnover rate than AT, and the niche breadth of RT was significantly narrower than that of AT. In comparison with AT, RT presented stronger phylogenetic signals for ecological preferences across environmental gradients. Null model analyses revealed that RT were more phylogenetically clustered and primarily governed by homogeneous selection, while AT were more overdispersed and dominated by dispersal limitation. Soil water content was the most decisive factor for community turnover and assembly processes of both AT and RT. Structural equation modeling analysis showed that RT were strongly associated with K. obovata biomass rather than S. alterniflora biomass, suggesting a strong relationship between RT and the growth of mangrove K. obovata Overall, our study revealed distinct assembly processes of soil AT and RT communities in coastal wetlands, which is crucial for mechanistic understanding of the establishment and maintenance of soil microbial diversity in coastal wetlands under conditions of global environmental changes.IMPORTANCE Coastal wetlands are one of the important ecosystems that play a crucial role in the regulation of climate change. Rare taxa (RT) exist in one habitat along with abundant taxa (AT). In this study, we found that RT exhibited narrower niche breadth and stronger phylogenetic signals than AT. Null model analyses showed that RT were more phylogenetically clustered and primarily governed by homogeneous selection, while AT were more overdispersed and dominated by dispersal limitation. Revealing the differences in the community assembly processes between AT and RT in coastal wetlands is critical to understand the establishment and maintenance of soil microbial diversity in coastal wetlands with regard to environmental changes.

Project description:Sedimentary microorganisms play crucial roles in maintaining the functional stability of aquatic ecosystems. However, their taxonomic composition and assembly processes are not well known in estuarine-coastal margins because of their complex environment. We investigated microbial communities, co-occurrence relationships, and underlying mechanisms in 33 surface sediment samples collected in the Jiulong River Estuary and the Taiwan Strait to reveal their composition dynamics. The abundance, diversity, and composition of microorganisms demonstrated obvious spatial variables. Methanobacterium and Methanosarcina, as well as Candidatus_Nitrosopumilus and Nitrososphaeraceae were the main methanogenic and ammonia-oxidizing archaea, with an average abundance of more than 5.91% and 4.27%, respectively. Along with a salinity gradient increase, the relative abundance of methanogenic archaea (from 42.9% to 16.6%) contrasted with the trend of ammonia-oxidizing archaea (from 6.04% to 18.7%). The number of methanogenic archaea gradually decreased with increasing geographic distance (p < 0.05), whereas ammonia-oxidizing archaea showed no significant change (p > 0.05). In co-occurrence patterns, closer inter-taxa connections were observed among archaea-archaea and bacteria-bacteria than in archaea-bacteria, which indicated that coexistence within the same kingdom was greater than interaction between different kingdoms in shaping the community structure along the salinity gradient. Furthermore, null model analyses of the microbial community showed that undominated was the most prominent process, explaining over 44.9% of community variation, followed by heterogeneous selection and dispersal limitation, which contributed to 27.7% and 16.3%, respectively. We demonstrated that stochasticity, rather than determinism, regulates community assembly. These results further highlight that intra-kingdom co-occurrence and stochastic processes shape the structure and assembly of microbial communities in estuarine-coastal margins.

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Increasing Inundation Frequencies Enhance the Stochastic Process and Network Complexity of the Soil Archaeal Community in Coastal Wetlands.

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