Human activities have triggered substantial changes in global climate systems with a preternatural rate over the past two centuries, leading to massive CO₂ absorption by the world’s oceans and a reduction in the pH of seawater which is known as ocean acidification (Caldeira and Wickett, 2003; Orr et al., 2005). The partial pressure of atmospheric CO₂ (pCO₂) has increased by nearly 40% from the preindustrial period to the present day (about 400 μatm) and is predicted to reach approximately 1,000 μatm by the end of this century (Caldeira and Wickett, 2003; IPCC, 2013). Ocean uptake of CO₂ changes the equilibrium of the carbonate system, and the continued release of anthropogenic CO₂ may lead to another 0.3–0.4units decline in seawater pH globally by 2100 (Orr et al., 2005; IPCC, 2013). As the most complicated and productive ecosystems, coastal oceans generally consist of diversiform but tightly connected aquatic environments, such as rivers, estuaries, tidal wetlands, and sea margins, all of which are strongly influenced by climatic and anthropogenic factors (Cai et al., 2011; Melzner et al., 2012; Wallace et al., 2014). Recent syntheses of the air-sea CO₂ fluxes in coastal waters suggest that CO₂ uptake in coastal ecosystems has reached to 0.22–0.45 Pg C yr.⁻¹, which is expected to affect the global carbon flux (Cai et al., 2006; Bauer et al., 2013; Regnier et al., 2013). In addition to a large CO₂ sink for the atmosphere, ocean acidification in coastal habitats was also reported to be amplified by eutrophication and hypoxia, and these regions might be grimmer by future climate change than previously thought (Cai et al., 2011; Melzner et al., 2012; Wallace et al., 2014). Therefore, the subsequent effects of ocean acidification on coastal life have become one of the most important issues.

Microorganisms exist everywhere and are abundant in density and genetic diversity (Azam and Worden, 2004; Azam and Malfatti, 2007). It has been estimated that microorganisms account for more than two-thirds of marine biomass, despite their tiny size (Bar-On and Milo, 2019). Furthermore, they are key components of the marine food web and play crucial roles in marine ecosystem function and carbon cycling (Azam, 1998; Jiao et al., 2010). The responses of microorganisms to climate change (e.g., ocean acidification) will be pivotal for the marine food web and the biogeochemical cycle in the future ocean. The responses of cyanobacteria, as important primary producers in the ocean, to elevated pCO₂ have been investigated in terms of their growth rates, photosynthesis, carbon concentration mechanisms, and cellular affinities for inorganic carbon (Fu et al., 2007; Flombaum et al., 2013; Dutkiewicz et al., 2015; Hutchins and Fu, 2017; Ma and Wang, 2021). With a higher abundance than cyanobacteria by 1–2 orders of magnitude, heterotrophic bacteria play a major role in recycling dissolved organic carbon and nutrients through the microbial loop; however, far less studies were conducted on relationships between heterotrophic bacteria and ocean acidification than phytoplankton (Azam et al., 1983; Azam, 1998; Robinson and Ramaiah, 2011). Previous studies have shown that responses of bacterioplankton communities to elevated pCO₂ are diverse and complex and even conflicting. Bacterioplankton communities were found to be susceptible to changes in pCO₂ or pH in some studies that were reflected in abundance, diversity, or composition (Krause et al., 2012; Zhang et al., 2013; Xia et al., 2019; Aguayo et al., 2020; Crummett, 2020), whereas other studies reported negligible effects (Roy et al., 2013; Oliver et al., 2014; Wang et al., 2015). Take coastal ecosystems for example, microbial community from coastal ecosystem with naturally low pH (average=7.8) was still sensitive to acidification (Crummett, 2020). However, recent evidence demonstrated that bacterioplankton community from variable coastal ecosystem was relatively stable under elevated pCO₂ condition (Allen et al., 2020). The relationships between bacterioplankton communities and elevated pCO₂ were more likely to be associated with environmental characteristics, such as nutrients and temperature (Bergen et al., 2016; Sala and Aparicio, 2016; Allen et al., 2020; Wang et al., 2021). Nevertheless, most studies on this topic have been performed in mesotrophic high-latitude regions, especially the Arctic Ocean, while less investigations were conducted in eutrophic low- and middle-latitude coastal ecosystems.

As a subtropical coastal region, Xiamen Bay is characterized by the input of nutrient-rich freshwater from Jiulong River, intrusion of saltwater from the South China Sea, and inflow of artificial wastewater, as well as being affected by intensive human activities (Chen et al., 2013; Cai et al., 2016). The Xiamen coastal ecosystem has showed nutrient-enhanced eutrophication since mid-1990s because of its hydrographical setting (Chen et al., 2013; Cai et al., 2016; Fu et al., 2016). Analyses of the long-term variations in the concentrations of nutrients in Xiamen coastal seawater suggest that dissolved inorganic nitrogen and phosphate have increased by several fold over recent decades (Cai et al., 2016). A time series sampling investigation revealed that the concentration of dissolved organic matter has even in Xiamen coastal ecosystem (Chen et al., 2021b). And estuarine input contributed a mass of dissolved organic matter, including humic-like fluorescent dissolved organic matter, S-containing, and N-containing organic molecules, to the coastal ecosystem (Chen et al., 2021b). In addition to eutrophication, interactions between anthropogenic CO₂ emissions and local drivers in coastal ecosystems (such as eutrophication, hypoxia, and biological activities) result in complex regulation of the pH and carbon cycle in coastal waters (Cai et al., 2011; Melzner et al., 2012; Wallace et al., 2014). Analyses of the annual variations in water quality indices in Xiamen Bay from 1986 to 2007 revealed that the mean pH values ranged from 7.86 to 8.21 and continuously decreased (Cai et al., 2016). To investigate the effects of elevated pCO₂ on bacterioplankton community at such a changing environment, a 5-day microcosm incubation experiment with eutrophic coastal water from Xiamen Bay under elevated pCO₂ and ambient conditions was conducted. During the incubation, the response of bacterioplankton community structure to elevated CO₂ and the population size of bacterioplankton were continuously detected.

Our results showed that both the population size and community structure of bacterioplankton were not significantly affected by elevated pCO₂ during 5-days of incubation, indicating that the bacterioplankton community in the coastal Xiamen Bay ecosystem was adaptable to the short-term elevated pCO₂. Similar results were also observed in earlier investigations (Grossart et al., 2006; Newbold et al., 2012; Oliver et al., 2014). For instance, elevated pCO₂ did not significantly affect the total bacterial cell count distributions in a marine picoplankton community under phytoplankton pre-bloom and post-bloom conditions (Newbold et al., 2012). Bacterioplankton communities were found to be highly resistant to short-term catastrophic pCO₂ perturbation in a mesocosm experiment, and no significant differences in community abundance, structure, or composition were observed (Oliver et al., 2014).

Recently, a hypothesis was re-proposed that environmental stability might influence the sensitivity of the bacterioplankton community to climate change (Liu et al., 2010; Joint et al., 2011; Wang et al., 2021). In other words, many bacterioplankton communities are already adapted to changing environments due to long-term exposure to variable environmental conditions and subsequent influence. The evidence to date suggests that coastal communities might be more resistant or flexible under changing environmental conditions than communities in more stable environments such as open ocean gyres (Wang et al., 2021). In addition, many studies have detected minor effects of elevated pCO₂ on bacterial abundance, while only few studies showed statistical significant responses which were mainly conducted in oligotrophic oceans, implying that nutrients might be an important influence on the relationship between bacterial population size and elevated pCO₂ (Grossart et al., 2006; Allgaier et al., 2008; Newbold et al., 2012; Maas et al., 2013; Bergen et al., 2016; Lin et al., 2018; James et al., 2019; Xia et al., 2019; Allen et al., 2020; Crummett, 2020; Hu et al., 2021). Similarly, significant impacts of elevated pCO₂ on bacterioplankton community diversity and composition also have been reported to be associated with nutrient regimes (Roy et al., 2013; Sala and Aparicio, 2016; Allen et al., 2020). By way of illustration, bacterioplankton community composition changed consistently in response to elevated pCO₂ at the ultra-oligotrophic center of the South Pacific gyre, while no significant pCO₂ treatment effect was found at the mesotrophic fringe of the South Pacific gyre (Allen et al., 2020). In general, therefore, it seems that bacterioplankton communities from coastal ecosystems were more stable in response to elevated pCO₂ and these ecosystems were always characterized as rapidly changing and eutrophic.

The Xiamen coastal ecosystem is a typical subtropical coastal ecosystem that is subjected to complex geographical and environmental influences. One of the consequences caused by anthropogenic activities and hydrological factors was the drastic pH fluctuation in Xiamen coastal ecosystem. The highest pH value of Xiamen coastal water has exceeded 8.5, and the lowest was under 7.5 for the last few decades (Cai et al., 2016). In addition, the probability of acid rain in Xiamen reached up to 68.8%, and this might also contribute to the low pH of the seawater.¹ Therefore, the bacterioplankton community in the Xiamen coastal region has already experienced the average surface ocean pH predicted to occur at the end of the century or even lower. Previous studies showed that the bacterioplankton community composition in an elevated pCO₂ mesocosm would be more conserved through time and resistant to CO₂ perturbation (Oliver et al., 2014). In addition, the variable pH in coastal ecosystems should also consider the effects of biological activity although the changes might be contrary to expectation in the future ocean. Biological driven diel fluctuations in pH could reach to 0.3–0.5 pH units in coastal ecosystems and even exceed 0.5 pH units during phytoplankton blooms or red tides (Joint et al., 2011; Hendriks et al., 2015). According to the records of red tide outbreak in the Xiamen coastal ecosystem, a total of 53 red tide events were recorded from 1986 to 2017 (Chen et al., 2021a). All these evidence indicated that the Xiamen coastal seawater has undergo drastic pH fluctuations on daily, seasonal, and even inter-annual scales. The coastal bacterioplankton communities in this area have probably adapted to these changes through processes including physiological acclimation and evolution (Evans and Hofmann, 2012). Moreover, as a result of the complexity and fluctuation in coastal habitats, bacterioplankton communities in coastal ecosystems were suggested to be highly variable reflecting the heterogeneity. And this heterogeneity might play a role in community stability (Zinger et al., 2011; Shade et al., 2012).

Prior studies have also noted the importance of trophic states in the response of the bacterioplankton community to ocean acidification. Bacterioplankton communities were suggested to be more resistant to ocean acidification in nutrient-rich waters (Roy et al., 2013; Sala and Aparicio, 2016; Allen et al., 2020). There was an experimental demonstration of the trophic effect in response of bacterioplankton to elevated pCO₂ revealed that more pronounced pH homeostasis genes were aroused to cope with pH stress in oligotrophic marine environments compared with high-nutrient conditions (Bunse et al., 2016). Additionally, the high expression levels of pH homeostasis genes in some bacterial groups are at the expense of growth, and this can ultimately affect the composition and diversity of the bacterioplankton community (Bunse et al., 2016; Allen et al., 2020). However, the energy cost of pH homeostasis expression was not necessary for bacterial cells in eutrophic oceans. The evidence thus far supports the idea that physiological acclimation of the bacterioplankton community to elevated pCO₂ is highly possible in eutrophic and highly changeable primitive environments.

Our results differ from those of a previous study on phytoplankton from the Xiamen nearshore, which showed that CO₂ enrichment enhanced the relative abundance of Flavobacteria during the early stage of a phytoplankton bloom (Lin et al., 2018). Notably, we used in situ bacterioplankton communities in our study, while the previous study introduced an artificial phytoplankton community into mesocosms system and conducted the incubation for a longer period (Lin et al., 2018). Therefore, one explanation for the differences in results might be that our 5-day incubation was too short to detect the long-term responses of the bacterioplankton community to seawater acidification, since Flavobacteria only showed increased relative abundance in the HC treatments at day 10 in the study of Lin et al. (2018). Another possible explanation is that artificial phytoplankton inoculated in the mesocosms influenced the competitive ability of Flavobacteria group at high pCO₂ level. In addition, the possible interference of bacterial community (including Flavobacteria) of the inoculated phytoplankton cultures could not be ruled out although the authors thought natural bacterioplankton was the determiner of responses to different CO₂ concentrations.

Bacterioplankton communities response to elevated pCO₂ in coastal regions are supposed to be foresight and important. Our results suggest the bacterioplankton community in the coastal region of Xiamen appears to be adaptable to the short-term elevated pCO₂ on account of the eutrophic and changeable habitat. To understand the ecological processes and mechanism underlined these phenomena, better experimental setup (e.g., >3 replicates), more comprehensive analysis of relevant environmental parameters (such as dynamics of organic and inorganic nutrients) and including other ecological components (e.g., heterotrophic nanoflagellates and phytoplankton) are required. In addition, given the influences of long-term environmental exposures on microbial phenotypic plasticity, acclimation, and evolutionary adaptation, this study cannot rule out the long-term effects of ocean acidification on coastal bacterioplankton communities. Thus, further experimentation at multiple temporal scales are needed to address issues related to acclimation and adaptation. Considering the diversification of coastal marine ecosystems caused by specific hydrogeological conditions and anthropogenic activities, predicting how coastal bacterioplankton communities will respond to elevated pCO₂ requires more investigations in more coastal ecosystems. Overall, the findings of this study contribute to our knowledge of bacterioplankton community responses to ocean acidification in coastal area and highlight the need for further research toward to understanding the long-term effects of ocean acidification on dynamic coastal ecosystems.

The data presented in the study are deposited in the national center for biotechnology information (NCBI) sequence read archive (SRA) repository, accession numbers SRR14766467–SRR14766473 (BioProject accession number PRJNA736025; BioSample accession numbers SAMN19606215–SAMN19606221). The names of the repository/repositories and accession number(s) can be found at: https://www.ncbi.nlm.nih.gov/sra/PRJNA736025, PRJNA736025.

RZ and NJ supervised the project and revised manuscript. FZ and YY performed the experiments. YY, FZ, XC, HL, and RZ analyzed data and wrote the manuscript. All authors interpreted the data and gave comments on the manuscript.

This study was supported by the National Key Research and Development Program of China (2020YFA0608300, 2021YFE0193000), National Natural Science Foundation (41861144018), China Postdoctoral Science Foundation (2019 M662237), the Senior User Project of RV KEXUE (KEXUE2020G10) from Center for Ocean Mega-Science, Chinese Academy of Sciences, and China Scholarship Council.

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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