Lagoon is a highly productive ecosystem that plays important ecological roles, such as biogeochemical element cycling, coastal biodiversity and blue carbon sequestration (Bhatnagar et al., 2020). The status of lagoon may vary in response to natural events and human activities (Duran et al., 2015). Microbial community shaped biogeochemical cycle, they drive carbon cycling in lagoon sediments, mediate mineral nutrition of sea plants, and alleviate carbon limitations of other sediment organisms. The activity of microbial community is crucial for carbon, nitrogen, and phosphorus cycling (Mohit et al., 2014), as well as determines the fate of nutrition (Bordenave et al., 2004a,b; Pringault et al., 2008; Stauffert et al., 2013; M’rassi et al., 2015).

More insights in the microbial community are critical for understanding the functions of lagoon ecosystem. For instance, Sáenz de Miera et al. (2021) reported that the seasonal disturbance of water level cycles is the major determinant of microbial community structure in sediments of saline lagoons located in the northwest of Spain. Ben Salem et al. (2019) revealed bacterial community assemblages in sediments under high anthropogenic pressure at Bizerte Lagoon hydrological system, Tunisia. Proteobacteria, Bacteroidetes, Chloroflexi, Planctomycetes, and Nitrospirae are the major phyla, which is consistent with previous observations in sediment environments (Behera et al., 2017; Fan et al., 2017). Besides the popularly abundant phyla Proteobacteria, Chloroflexi and Planctomycetes, Spirochaetes were also found in the sediment of an enclosed shallow coastal lagoon, Magdalen Islands, Gulf of St. Lawrence, Canada (Mohit et al., 2015).

As a matter of fact, coastal lagoons usually have strong physicochemical gradient of salinity, nutrient concentration, turbidity, and organic matter content. The diversity of microorganisms in these ecosystems indicates that microbial community can be shaped by a variety of environmental factors, such as salinity, temperature, pH, hydrology, and latitude (Mohit et al., 2014). A previous study has revealed the environmental factors controlling the bacterial abundance in the sediments of a Mediterranean lagoon ecosystem. In this study, the variation of bacterial distribution was related to abiotic (temperature, ammonium, and pH) and trophic parameters (such as chlorophyll a) (Pala et al., 2018). An association analysis between sediment bacterial communities and environmental factors in Intermittently Closed and Open Lakes and Lagoons (ICOLLs) revealed that the bacterial diversity in Manly may be due to eutrophication, and that in Narrabeen may be attributed to the variety of organic matter sources (Filippini et al., 2019). Another study investigated the bacterial diversity and microbial functional response to organic matter composition in deltaic lagoon sediments, finding that at low organic contamination levels, the riverine inputs provide additional bioavailable carbon sources without evident adverse effects (Zoppini et al., 2020).

Coastal lagoon and the surrounding area are important aquatic systems with strong physicochemical gradients, where microorganisms have been well recognized to participate in biogeochemical cycles (Mary et al., 2014). However, the microbial composition, distribution and function in these environments remain largely unknown in the South China Sea. In this study, we investigated the microbial community in Qilianyu lagoon of China by analyzing the microorganisms involved in the regulation of microbial community structure with high-throughput sequencing, and systematically studying the correlation between microorganisms and physicochemical characteristics.

Proteobacteria are frequently reported as the dominant phyla in lagoon sediments, and microbial composition will change according to their geographical location (Behera et al., 2017). Zoppini et al. (2020) found that Proteobacteria and Bacteroidetes were dominant in the deltaic lagoon sediments of Italy, followed by Epsilonbacteraeota, Firmicutes, Chloroflexi, Planctomycetes and Verrucomicrobia. A previous study investigated the benthic sediment bacteria in Celestún Lagoon in the Southern Gulf of Mexico. The results revealed that Proteobacteria, Chloroflexi, Bacteroidetes and Planctomycetes are the dominant taxa, followed by Spirochaetae, Acidobacteria, Actinobacteria, Cyanobacteria and Verrucomicrobia (Cadena et al., 2019). Sáenz de Miera et al. (2021) collected sediments from four lagoons of Spain, including Barillos, Salina Grande, Villarrin and Villalpando. Proteobacteria was identified as the most abundant phylum in all lagoons, except for Grande, where Chloroflexi was more abundant than Proteobacteria despite insignificant differences. The popular marine bacteria Proteobacteria were also found to be dominant in the sediments of Qilianyu lagoon. However, the order of other bacterial phyla in Qilianyu lagoon was different from that in the aforementioned lagoons. For fungi, ITS1 sequences of sediments collected from a coastal lagoon connected as a subestuary to Waquoit Bay (Cape Cod, MA, United States) were identified to be associated with Ascomycete, Chytridiomycota, Sordariomycetes, Pleosporales and Agaricomycetes. Typically, the sediments were dominated by the ascomycete genus Orbilia, which is different from the case of Qilianyu lagoon where Aspergillus is the main genus (Ortega-Arbulú et al., 2019). These results indicate that the divergence of bacterial and fungal composition in the sediments is affected by the geographical location.

Previous studies have identified total organic carbon as one of the most important factors affecting the bacterial composition in different aquatic habitats (Lallias et al., 2015; Highton et al., 2016). The relative abundance of bacterial taxa increased with total organic carbon increasing. These bacteria include Candidatus Giovannonibacteria (GW2011_GWB1_47_6b), Candidate division CPR3 (GW2011_GWF2_35_18), Parcubacteria (group bacterium ADurb. Bin326), Deferribacteraceae, Chlorobiaceae and Bradyamonadaceae (Filippini et al., 2019). A study of Chilika Lagoon located along the east coast of India also revealed the environmental conditions affected the microbial difference. The bacterial taxa include α-Proteobacteria, γ-Proteobacteria, Sphingobacteria, Bacilli, Nitrospira and Acidobacteria_Gp10, which prefer the higher salinity regime in the lagoon. In contrast, β-Proteobacteria, Clostridia and Actinobacteria prefer the freshwater-brackish salinity regime. However, none of the sediment parameters (total organic carbon, total nitrogen, total phosphorus, and pH) measured in the Chilika Lagoon was significantly correlated with the bacterial community composition (Behera et al., 2017). Here, we found that organic matter and total nitrogen exhibited positive relationships with Xenococcus, whereas had no linear relationship with Pleurocapsa. Our results suggest that natural changes in organic and nitrogen enrichment in the sediments can regulate the Xenococcus in Qilianyu lagoon.

Xenococcus classified in the phyla Cyanobacteria, it is widely found in the ocean ecology, but their biogeography and functions in lagoon environments is poorly understood. A case study of the Golden Bay mangrove in China demonstrated that cyanobacterial assemblages were dominated by Synechococcus and Xenococcaceae, and there was a clear shift of dominance from Synechococcus to Xenococcaceae toward the sea (Zhu et al., 2018). Rigonato et al. (2013) revealed that most of cyanobacteria were uncultivated (unclassified) and only a few Xenococcus sequences were detected in the mangrove soils in south-east Brazil. However, Xenococcus species have been detected on the trunks, roots, and pneumatophores of several mangrove trees (including Avicennia marina) with morphology-based methods (Alvarenga et al., 2015). Xenococcus was also found in the intertidal zones of the Portuguese coast, and in cyanobacterial mats retrieved from the La Réunion lagoon (Brito et al., 2012; Echenique-Subiabre et al., 2015). These results indicate the ubiquity of Xenococcus in the marine environment. Xenococcus one of genus of Cyanobacteria, and many research showed that Cyanobacteria play an important role in balance of nutrients, primarily carbon and nitrogen of marine ecosystems (Al-Thukair et al., 2007; Charpy et al., 2012). In this research, we also found that organic matter and total nitrogen could significantly regulate the relative abundance of Xenococcus. Furthermore, Xenococcus was found to affect the bacterial and fungal community structure in the sediments. Therefore, changes in organic matter and total nitrogen may lead to the differences in microbial community structure of the sediments between the lagoon and surrounding areas through the regulation of Xenococcus abundance.

This study analyzed the physicochemical characteristics and microorganisms in the lagoon and surrounding areas, which is beneficial to further understand the ecological characteristics of Qilianyu lagoon. The results indicate that organic matter and total nitrogen lead to the differences in microbial community structure in sediments between the lagoon and surrounding areas through the regulation of Xenococcus abundance. In the future, further research can be focused on whether fungi are involved in the regulation of the microbial community structure and the bacterial regulation mechanism.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/Supplementary Material.

YC: software. YQ, HW, and HL: formal analysis. YC, MZ, YQ, HW, and QT: investigation. YC, MZ, and HZ: writing – original draft preparation. YC and ZZ: writing, review, editing, project administration, and funding acquisition. ZZ: supervision. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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