Original Research ArticleTemporal change of prokaryotic community in surface sediments of the Chukchi Sea
Introduction
Marine microbes play vital roles in maintaining the stability of marine ecosystem and driving the geochemical elements circulation of the earth (Sala et al., 2010; Zeng et al., 2013). However, microbial diversity, community structure and even assembly processes are influenced by environmental disturbance (Choi et al., 2016; Liu et al., 2021; Wang et al., 2016). It was reported that the Arctic Ocean was warming faster than the rest of the planet, and lead to marine environment changing rapidly in the last decades (Abirami et al., 2021; Cardozo-Mino et al., 2021). Previous studies indicated that marine microorganisms respond to high or low-frequency variations in the marine environment with shifting in abundance and community structure that have implications for their ecosystem function (Bar-On et al., 2018; Wang et al., 2020; Wilson et al., 2021). However, most previous studies about prokaryotes had only focused on freshwater systems or coastal areas of their composition and spatial distribution (Didier et al., 2017; Grossmann et al., 2016; Wilson et al., 2021; Zhong et al., 2016). Marine sediments, as one of the most special habitats which were relatively independent of upper seawater environment and receiving vertical exportation of inorganic and organic matters from upper water layer, have been rarely explored (Bunse and Pinhassi, 2017; Caporaso et al., 2011; Fuhrman et al., 2015).
Understanding the processes and mechanisms controlling community assembly is a central topic in ecology, particularly in microbial ecology (Zhou et al., 2017). Community assembly processes determines the composition and diversity of microbial community, and then govern its functions (Zhang et al., 2019). Therefore, the focus of microbial ecology has shifted from geographic distribution to underlying microbial assembly processes in recent years (Hanson et al., 2012; Wang et al., 2020). Pioneers thought that although stochastic processes are believed to play non-negligible roles in shaping community structure, their relative importance over deterministic processes are hotly debated (Dini-Andreote et al., 2015; Stegen et al., 2016; Zhou et al., 2013), because traditional niche-based theory hypothesizes that deterministic factors and environmental conditions are also key factors dominating the community structure (Fargione et al., 2003). Currently, it is recognized that community assembly is simultaneously influenced by both deterministic and stochastic processes (Chase and Myers, 2011; Stegen et al., 2012). However, little is known about the relative contribution of different ecological processes in governing the assembly of microbial communities in marine sediments.
Uncovering species coexistence in microbial communities is also an enduring challenge for microbial ecologists (Chen and Wen, 2020). Network analysis has been well used to explore microbial interactions and/or symbiotic patterns among different microbial taxa in various environments (Banerjee et al., 2018; Röttjers and Faust, 2018). The co-occurrence patterns illustrated by a network capture important information in microbial ecology under this method, such as microbial taxa are linked together either positively or negatively (Liu et al., 2019). Numerous studies have used network-based scores to identify putative keystone taxa in various environments (Banerjee et al., 2018; Chen and Wen, 2020; Liu et al., 2020). However, some earlier studies indicated that keystone taxa that were not numerically dominant in the communities have been identified in the Arctic ecosystem (Comte et al., 2016; Gokul et al., 2016; Hill et al., 2016) and Antarctic ecosystem (Vick-Majors et al., 2014). Therefore, it remains to clear whether microbial co-occurrence relationships exhibit temporal patterns and whether their dynamics are associated with variations in community composition (Liu et al., 2020).
The year of 2016 was the second warmest year on record since record-keeping began in 1850 (+ 1.02 °C temperature anomaly, Fig. S1), which was 0.25 °C higher than 2014 (+ 0.77 °C temperature anomaly) on average. Global warming may alter microbial mediated ecosystem functions through reshaping of microbial diversity and modified microbial interactions in a long term (Zhou et al., 2021). And some studies found that prokaryotic diversity and composition would change due to environmental conditions changed in a long time scale (over 5 or 10 years) (Cram et al., 2015; Parada and Fuhrman, 2017), and climate warming was one of the main driven factors (Abirami et al., 2021; Neukermans et al., 2018; Shi et al., 2018; Timmermans and Marshall, 2020). But it is not clear whether climate warming would lead to significant environmental change and prokaryotic shift in the marine sediment ecosystem in a relative short time.
The Chukchi Sea is a marginal sea of the Arctic Ocean, located northeast of the Asian continent and northwest of the North American continent. It has Wrangel Island in the west, Beaufort Sea in the east, The Pacific Ocean in the south via the Bering Strait, and the Arctic Ocean in the north. It has a special geographical location and significantly affected by human activities, which making it as an ideal area for exploring microbial responses to climate change. Therefore, in this study, the changes of bacterial and archaeal communities in the Chukchi Sea were investigated based on amplicon sequencing. Ultimately, several environmental parameters were characterized to explain the prokaryotic community variation. In this study, we aim to figure out that (i) whether the sedimental characteristics changed significantly or not within only two warming years? (ii) how the prokaryotic diversities and community compositions changed from 2014 to 2016? (iii) whether and how natural climate warming affects the prokaryotic community assembly and the complexity of prokaryotic co-occurrence networks?
Section snippets
Study site, sampling, and physicochemical analysis
Sediments were sampled from 10 sites which were set in the Chukchi Sea, during the 6th and 7th Chinese National Arctic Research Expedition (in the year of 2014 and 2016, respectively). Sampling sites were shown in Fig. 1. Sediments samples were collected by undisturbed box cores (50 × 50 × 65 cm). After retrieval, the top 5 cm of sediments were transferred to sterile tubes. All of the samples were immediately flash-frozen in liquid nitrogen, and then stored at -80 °C until DNA extraction. Some
Physicochemical properties of samples
The physicochemical properties of sediments were measured and summarized in Table S1. Overall, the sampling depth was about 50-meter depth except R10, R11 and R13, the pH value was at the range of 7.15∼8.33, pH values had significantly decreased from 2104 to 2016 (P = 0.008 < 0.01, T-test, Table S2). The contents of TN were at the range of 1.2-11.6 g/Kg in 2014 and 2016, and most samples were lower than 5 g/Kg. The contents of TP were higher than 207.92 mg/kg in all samples, and the contents of
Discussion
Marine sediments are the largest sedimental environment and are populated by a diverse microbial community, and play irreplaceable role on geochemical elements cycling on the planet. A multitude of concurrent biological and physical processes contribute to microbial community turnover, especially in marine systems (Wilson et al., 2021). Investigation of bacterial and archaeal diversity and community dynamics across different time is important for understanding how prokaryotic change over time.
Conclusions
Long-term climate warming on our planet caused significant environmental changes and have strong impacts on microorganisms, even in marine benthic environment. However, it is unclear whether the microbial changes are significant in a shorter term. In this study, our results indicated that prokaryotic diversity increased from 2014 to 2016 and the composition of prokaryotes fluctuated markedly. Moreover, compared with archaea, bacterial community assembly processes were shift from stochasticity
CRediT authorship contribution statement
Jianxing Sun: Software, Validation, Writing – review & editing. Hongbo Zhou: Writing – review & editing. Haina Cheng: Software, Methodology. Zhu Chen: Data curation, Writing – review & editing. Yuguang Wang: Resources, Conceptualization, Funding acquisition.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Consent to publish
All authors have given their consent to publish this research article.
Acknowledgments
This study was supported by the National Nature Science Foundation of China (41706221 and 42073079). We greatly appreciated that Professor Ye Deng and Professor Jizhong Zhou provided the pipeline (Metagenomics for Environmental Microbiology, http://mem.rcees.ac.cn:8080/ and the Molecular Ecological Network Analyses Pipeline, http://ieg4.rccc.ou.edu/MENA/) for our data processing.
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