Temporal change of prokaryotic community in surface sediments of the Chukchi Sea

Abstract

Global warming may alter microbial ecosystem functions through reshaping of microbial diversities, compositions and interactions. Here, the community compositions, assembly processes and microbial interactions of prokaryotes (bacteria and archaea) were compared between the warming year of 2014 and 2016 in the Chukchi Sea. Our results indicated that prokaryotic diversity was significant higher in the warmer year of 2016. Furthermore, stochastic processes always dominated archaeal assembly processes, but bacterial assembly processes were mainly shaped by deterministic processes in 2016. And more keystones were detected in bacteria than that in archaea to maintain prokaryotic community stability. Both bacterial and archaeal community variations had significant correlations with environmental factors, although many of these factors (such as TN, TP, TOC and heavy metals) had not changed significantly from 2014 to 2016. Our study provides some new insights into microbial responses to climate warming in marine sediments.

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?