The establishment of coastal embankments significantly decreased the Simpson diversity index in the S. alterniflora salt marsh, while they increased the OTU richness in the P. australis salt marsh (Fig. 2). Interestingly, coastal embankments altered the microbial diversity and richness only slightly in the 0–30 cm soil layer of the S. salsa salt marsh (p ≥ 0.05; Fig. 2). Soil nutrient substrates (e.g., SOC and SON) provide media for the presence of microbes and, as such, are critical drivers of soil bacterial and archaeal diversity and richness (Yu et al. 2019; Gao et al. 2020; Novoa et al. 2020; Yang et al. 2020).
In this study, the soil bacterial and archaeal diversity were highly positively correlated with the SOC, ROC, SON, LON, and RON in the soil (Table S2). The accumulation of nutrients in the soil is primarily determined by the quantity and quality of plant residue inputs (Chantigny 2003; Belay-Tedla et al. 2009; Yang et al. 2016). The low soil salinity (e.g., 2.399‰) of the embanked S. alterniflora salt marsh created difficulties for this plant to complete its life cycle. As the establishment of coastal embankments limited the growth of S. alterniflora (Tables 1 and S2; Fierer and Jackson 2006; Zhong et al. 2011; Zhao et al. 2020), the decrease in plant residue biomass led to lower SOC, ROC, SON, LON, and RON in the soil of the embanked S. alterniflora salt marsh, which ultimately diminished the diversity of the soil bacteria and archaea (Tables 1, 2 and S2; Yang et al. 2016; Yu et al. 2019).
Conversely, the lower soil salinity (e.g., 1.737‰) in the embanked salt marsh was more suitable for the growth of P. australis than the high soil salinity (e.g., 4.164‰) of the unembanked salt marsh (Table 1). The increased residue biomass of P. australis caused by the low soil salinity led to an increase in the SOC and SON of the embanked P. australis salt marsh, which presumptively increased the OTU richness (Tables 1 and 2; Yang et al. 2020). However, coastal embankments had insignificant impacts on plant residues, as well as soil SOC, LOC, WSOC, SON, LON, and WSON in the S. salsa salt marsh, which explained the negligible impact of these structures on bacterial and archaeal diversity and richness in the S. salsa salt marsh (Fig. 2; Table 2).
Soil moisture is a vital driver of soil bacterial and archaeal diversity (Guo and Zhou 2020; Yang et al. 2020; Sun et al. 2021). Previous studies reported that the higher availability of soil water in coastal zones was advantageous for the diversity of soil bacteria and archaea in these areas, which was consistent with the results of this study (Table S2; Gao et al. 2020; Novoa et al. 2020). The embankments prevented seawater from reaching the coastal wetlands, which decreased the soil moisture of the S. alterniflora salt marsh, thereby contributing to lower diversity (Table 2). However, the probable presence of aquifers within the embanked soil and precipitation can decrease the impact of embankments (Guo and Jiao 2007; Yang et al. 2016; Ma et al. 2019).
In this study, the soil moisture was increased in the embanked P. australis salt marsh, which might have explained its higher OTU richness (Fig. 2; Table 2). Soil pH shows an excellent correlation with bacterial and archaeal diversity; however, in our study, an insignificant correlation was observed between the soil pH and bacterial and archaeal diversity (Table 2). In summary, our results indicated that the establishment of coastal embankments influenced the bacterial and archaeal diversity and richness in S. alterniflora and P. australis communities by shifting soil nutrient substrates, which was primarily determined by plant residues, and changes in soil moisture (Tables 1, 2 and S2).
The establishment of coastal embankments drastically modified the composition of soil bacterial and archaeal communities in S. alterniflora and P. australis salt marshes (Fig. 5). PCoA and Bray-Curtis dissimilarity indices revealed that the soil bacterial and archaeal community compositions in the embanked S. alterniflora and P. australis salt marshes were clustered and distinct from those in the unembanked S. alterniflora and P. australis salt marshes, respectively (Fig. 5). However, the variation in the compositions of soil bacterial and archaeal populations between the unembanked and embanked S. salsa communities was insignificant (Fig. 5).
The WSOC, which is the first to be rapidly utilized by bacteria and archaea, was the most direct driver of soil bacterial and archaeal community composition among the different plant communities in the coastal wetlands. This was because the variations in the soil bacterial and archaeal communities were intimately related to the WSOC at the class, order, family, and genus levels (Figs. 6 and S2; Orwin et al. 2016; Santonja et al. 2017; Yang et al. 2020). Additionally, RON, which represents available nutrients, vitally influenced the composition of the bacterial and archaeal communities among the different plant communities (Figs. 6 and S2; Bates et al. 2011; Yang et al. 2020; Rasmussen et al. 2021).
Thus, in this study, the decrease of WSOC and RON in the S. alterniflora salt marsh following the establishment of coastal embankments caused a differentiation in the bacterial and archaeal communities between the unembanked and embanked S. alterniflora salt marshes (Figs. 5, 6 and S2; Table 2). Additionally, the higher concentrations of WSOC and RON in the embanked P. australis salt marsh influenced the differentiation of the bacterial and archaeal communities between the unembanked and embanked P. australis salt marshes (Figs. 5, 6 and S2; Table 2).
Furthermore, the insignificant difference in soil nutrient substrates explained the inconspicuous differentiation of bacterial and archaeal communities between the unembanked and embanked S. salsa salt marshes (Figs. 5, 6 and S2; Table 2). Besides, the microbial community composition was also primarily influenced by changes in the soil C/N ratio (Fig. 6). An increased C/N ratio typically suggests that soils are degraded due to the loss of C, which limits microbial growth (Pereira et al. 2021). However, in this study, embankments did not change the soil C/N ratio for all vegetation types; thus, they did not modify the microbial community composition by altering the soil C/N ratio (Table 2).
Consequently, our results confirmed that the establishment of coastal embankments influenced the soil bacterial and archaeal community composition primarily by altering the concentrations of nutrient substrates, which was determined significantly by plant residues (Fig. 7; Table 2; Liao et al. 2007; Yang et al. 2016). In this study, the establishment of coastal embankments had a negligible effect on the relative archaeal abundance at the phylum, class, order, family, genus, and species levels (Table S5). As archaea are extremophilic microorganisms, few environmental factors can have dramatic impacts on their growth, which might explain these results (Bates et al. 2011; Ventosa and Haba 2011).
Several chemoorganotrophic bacteria were significantly influenced following the establishment of embankments. The phylum proteobacteria has been described in marine and terrestrial ecosystems as an important component of biogeochemical cycles, and was the most abundant phylum in the sediment of coastal Yancheng (Fig. S3; Lee et al. 2020; Yang et al. 2020). In this study, the class Gammaproteobacteria was the most abundant, and its relative abundance was influenced markedly following the establishment of embankments (Figs. 3 and S3).
The coastal embankment dramatically simulated the presence of Gammaprotebacteria in S. salsa saltmarshes (Fig. 3). Moreover, the abundance of Gammaproteobacteria in the embanked S. salsa saltmarsh was much higher than those in the other saltmarshes (Fig. 3; Table S3). Gammaproteobacteria is classified as a copiotrophic bacterial taxon, which has the capacity to grow quickly by utilizing labile compounds, particularly dissolved organic matter (Wang et al. 2020; Figueroa et al. 2021; Tian et al. 2021). Previous studies reported that S. salsa litter had lower lignin concentrations than that of S. alterniflora and P. australis. A lower lignin concentration translated to a faster passive release of labile compounds from the S. salsa litter (Cui et al. 2019; Trevathan-Tackett et al. 2020).
In this study, we also observed that S. salsa saltmarshes possessed higher WSON concentrations than S. alterniflora saltmarshes, and higher WSOC concentrations than P. australis saltmarshes (Table S1). The high WSOC and WSON concentrations increased the presence of Gammaproteobacteria in the S. salsa saltmarsh (Cleveland et al. 2007; Han et al. 2021). Additionally, when the supply of dissolved organic matter is sufficient Gammaproteobacteria will grow better under stable water conditions (Figueroa et al. 2021). The coastal embankment blocked the tide water, which provided a stable water supply and further improved the presence of Gammaproteobacteria in the S. salsa saltmarsh.
The class of Deltaproteobacteria is frequent in coastal sediments, and has been described as a degrader of recalcitrant compounds (Fig. S3; Fierer et al. 2007b; Liu et al. 2018; Trevathan-Tackett et al. 2020). Previous studies reported that several species of Deltaproteobacteria can even be isolated from recalcitrant crude oil (Acosta-González et al. 2013; Liu et al. 2018). In this study, SEM analysis also verified that the abundance of Deltaproteobacteria was highly correlated with ROC and RON concentrations in the soil (Fig. 7). Since S. alterniflora and P. australis residues are rich in lignin and lignocellulosic materials, the coastal embankments altered the inputs of recalcitrant materials from plant residues in the S. alterniflora and P. australis saltmarshes, which ultimately changed the ROC and RON concentrations in the soil (Ji et al. 2011; Cui et al. 2019; Yang et al. 2020).
Therefore, the coastal embankments decreased the quantities of plant residues, and soil ROC and RON, which resulted in the reduced abundance of Deltaproteobacteria in the S. alterniflora saltmarsh. The coastal embankments increased the amount of plant residues, as well as soil ROC and RON, which led to an increase in the abundance of Deltaproteobacteria in the P. australis saltmarsh (Tables 2 and S3). Similar to Deltaproteobacteria, we found that the abundances of Epsilonproteobacteria and Rhodothermi were obviously correlated with the ROC and RON concentrations, which supported the notion that Epsilonproteobacteria and Rhodothermi can break down refractory organic matters (Kirchman 2002; Kim and Kwon 2010; Lormieres and Oger 2017).
Thus, the coastal embankments had similar influences on Epsilonproteobacteria and Rhodothermi as on Deltaproteobacteria (Fig. 7). Moreover, some Actinobacteria are oligotrophic bacteria whose growth is restricted in nutrient-rich soils (Pascault et al. 2013; Trivedi et al. 2013; Verzeaux et al. 2016; Yang et al. 2020). Decreased S. alterniflora biomass in the soil of embanked salt marshes severely reduced the availability of nutrients (e.g., SOC and WSON), which was beneficial for the presence of Actinobacteria, and reduced its abundance in the embanked S. alterniflora sediment (Fig. 3; Tables 1 and 2). Thus, our results suggested that the establishment of coastal embankments influenced the distribution of chemoorganotrophic bacteria, as they modified the soil nutrient substrates (e.g., SOC, ROC, RON, and WSON) by appreciably altering the organic material inputs from plants.
Coastal embankments also affected the presence of photosynthetic bacteria by influencing plant growth. Photosynthetic bacteria are widely distributed in coastal sediments (Okubo et al. 2006; Idi et al. 2014). In this study, the quantity of obligately phototrophic bacteria from the phylum Chlorobi and class Chloroflexi (Garrity et al. 2005; Hanada 2014) was significantly higher in the embanked S. alterniflora salt marsh (Fig. 4). The light-limiting effect of the dense vegetation of S. alterniflora directly restricted the presence of PSB (He et al. 2012; Li et al. 2014b; Brotosudarmo et al. 2015).
Indeed, the abundances of the phylum Chlorobi and class Chloroflexi were significantly negatively correlated with the aboveground biomass of plants (Table S4). Thus, the higher occurrence of the phylum Chlorobi and class Chloroflexi might have been induced by the increased sunlight due to the lower aboveground biomass of plants in the embanked S. alterniflora salt marsh (Fig. 4; Tables 1 and S4; Wang et al. 2012). In contrast, the shade provided by the increased aboveground biomass of plants might explain the lower abundance of 4C0d-2, which are also obligately phototrophic bacteria in the embanked P. australis salt marsh (Fig. 4; Table 1).
Chromatiaceae, which is known as phototrophic purple sulfur bacteria, can grow via photolithoautotrophic metabolism (Imhoff 2005). In this study, the presence of Chromatiaceae was negatively correlated with the aboveground biomass of plants (Table S4). Thus, the decreased aboveground biomass of S. salsa in the embanked salt marsh explained the greater occurrence of Chromatiaceae in this environment (Tables 1 and S4). Generally, the establishment of coastal embankments affects the presence of PSB by primarily altering the aboveground biomass of plants.
Pathogenic bacteria target plant and animal species. In this study, the coastal embankments stimulated the presence of some pathogenic bacteria that most likely threatened plants, and even the health of the entire ecosystem (Dangl and Jones 2001; Glazebrook 2005). For example, Xanthomonadales are aerobic, and in this study, their abundance was significantly negatively correlated with soil salinity (Fig. 3; Bayer-Santos et al. 2019). The decreased soil moisture and salinity of the embanked S. alterniflora salt marsh created aerobic conditions with low salinity that ultimately promoted the presence of Xanthomonadales, particularly that of Xanthomonadaceae (Fig. 3; Table 2; Bayer-Santos et al. 2019).
Xanthomonadales includes several plant pathogens, especially those belonging to the family Xanthomonadaceae (Bayer-Santos et al. 2019). Therefore, coastal embankments showed limited S. alterniflora growth, and the increased presence Xanthomonadales would damage it even further. Pseudomonadales are chemoorganotrophic, and in this study, their abundance was positively correlated with the SOC concentration (Figs. 3 and 7; Palleroni 2005; Peix et al. 2009). The increased presence of Pseudomonadales in the embanked P. australis saltmarsh might be explained by the significant increase in SOC in this environment (Table 2). Pseudomonadales is pathogenic species that affect animals and plants (Palleroni 2005; Peix et al. 2009). Therefore, the increased Pseudomonadales in embanked P. australis saltmarsh not only harmed plants, but also had negative impacts on animal health. As the study area is the most important habitat of the endangered Red-crowned Crane, the increased abundance of pathogenic bacteria could put this species at risk.
Several bacterial groups were directly affected by the absence of seawater owing to the coastal embankments. In this study, the presence of Betaproteobacteria (a dominant class within Proteobacteria) was stimulated in the embanked regions for all vegetation types (Figs. 3 and 4; Tables 1 and 2). Additionally, in embanked regions, the abundance of Betaproteobacteria were more pronounced near to shore, rather than at more seaward locations (Table S3). Betaproteobacteria has been suggested to originate from freshwater or terrestrial ecosystems and is rarely found in seawater (Ruiz-González et al. 2015; Baña et al. 2020; Figueroa et al. 2021).
Indeed, in this study, the abundance of Betaproteobacteria was negatively correlated with soil salinity and positively related with the soil pH (Fig. 7). Therefore, we speculated that coastal embankments significantly reduced soil salinity and increased the pH by blocking seawater, which ultimately promoted the growth of Betaproteobacteria. However, Betaproteobacteria have been reported to be highly active in the decomposition of organic matter and can utilize fresh and labile substrates (Dai et al. 2021). Thus, more abundant Betaproteobacteria in the embanked regions might have given rise to losses in labile nutrients (Fig. 7). In conclusion, the establishment of coastal embankments strongly influenced the growth of some bacterial strains by stopping seawater from reaching the plant communities, and consequently changing the physicochemical soil properties, and varying bacterial populations may cause changes in the composition of soil nutrients.