Bacterioplankton community resilience to ocean acidification: evidence from microbial network analysis

ICES Journal of Marine Science ICES Journal of Marine Science (2016), 73(3), 865– 875. doi:10.1093/icesjms/fsv187 Contribution to Special Issue: ‘Towards a Broader Perspective on Ocean Acidification Research’ Original Article Bacterioplankton community resilience to ocean acidification: evidence from microbial network analysis Yu Wang 1‡, Rui Zhang 1‡, Qiang Zheng 1, Ye Deng 2, Joy D. Van Nostrand3, Jizhong Zhou 3,4,5*, and Nianzhi Jiao 1* 1 State Key Laboratory of Marine Environmental Science, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, Fujian 361005, People’s Republic of China 2 CAS Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, People’s Republic of China 3 Institute for Environmental Genomics and Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019, USA 4 State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment, Tsinghua University, Beijing 100084, China 5 Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA *Corresponding author: e-mail: (N.J.); (J.Z.) Equal contribution. ‡ Wang, Y., Zhang, R., Zheng, Q., Deng, Y., Van Nostrand, J. D., Zhou, J., and Jiao, N. Bacterioplankton community resilience to ocean acidification: evidence from microbial network analysis. – ICES Journal of Marine Science, 73: 865 –875. Received 7 April 2015; revised 22 August 2015; accepted 28 September 2015; advance access publication 20 November 2015. Ocean acidification (OA), caused by seawater CO2 uptake, has significant impacts on marine calcifying organisms and phototrophs. However, the response of bacterial communities, who play a crucial role in marine biogeochemical cycling, to OA is still not well understood. Previous studies have shown that the diversity and structure of microbial communities change undeterminably with elevated pCO2. Here, novel phylogenetic molecular ecological networks (pMENs) were employed to investigate the interactions of native bacterial communities in response to OA in the Arctic Ocean through a mesocosm experiment. The pMENs results were in line with the null hypothesis that elevated pCO2/pH does not affect biogeochemistry processes. The number of nodes within the pMENs and the connectivity of the bacterial communities were similar, despite increased pCO2 concentrations. Our results indicate that elevated pCO2 did not significantly affect microbial community structure and succession in the Arctic Ocean, suggesting bacterioplankton community resilience to elevated pCO2. The competitive interactions among the native bacterioplankton, as well as the modular community structure, may contribute to this resilience. This pMENs-based investigation of the interactions among microbial community members at different pCO2 concentrations provides a new insight into our understanding of how OA affects the microbial community. Keywords: Arctic Ocean, community structure, mesocosm experiment, molecular ecological network, ocean acidification. Introduction Since the industrial revolution, the impact of human activity on the global climate has increased greatly as a result of increasing carbon dioxide (CO2) emissions from anthropogenic sources. The uptake of anthropogenic carbon dioxide by the ocean has caused a decrease of pH 0.1 units (ocean acidification, OA; IPCC, 2015). Previous studies have demonstrated that some phototrophic communities, like sea grass (Zimmerman et al., 1997; Jiang et al., 2010), diatoms (Riebesell et al., 1993; Baragi et al., 2015; Taucher et al., 2015), and coccolithophorids (Hiwatari et al., 1995; Lv et al., 2015), have higher photosynthesis rates under a higher partial pressure of carbon dioxide (pCO2). However, the response of marine bacterioplankton, a crucial player in marine biogeochemical cycling (Azam, 1998; Jiao et al., 2010), to OA is not well understood at present. Joint et al. (2011) proposed that “marine microbes possess the flexibility to accommodate pH change”. Indeed, several mesocosm studies have found that elevated pCO2 has little effect on bacterial communities in the Arctic Ocean (Allgaier et al., 2008; Tanaka et al., 2008; # International Council for the Exploration of the Sea 2015. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 866 Oliver et al., 2014). The abundance and activity of bacteria in these communities did not differ statistically under three different pCO2 treatments (350, 700, and 1085 matm; Allgaier et al., 2008). Furthermore, phylogenetic diversity analysis revealed no clear effect of elevated pCO2 on a bacterioplankton assemblage in the high Arctic Ocean (Monier et al., 2014). In contrast, a few studies have demonstrated that elevated pCO2 has some influence on microbial community composition (Krause et al., 2012; Bowen et al., 2013). Other studies have also shown that the production and growth rates of bacterial isolates were strongly affected by high pCO2 and low pH (Takeuchi et al., 1997; Labare et al., 2010; Teira et al., 2012). For example, Vibrio alginolyticus growth was suppressed under low pCO2 levels (Michael et al., 2010). In contrast, high pCO2 stimulated the growth efficiency of one Flavobacteria strain (Teira et al., 2012). Moreover, the rate of microbial ammonia oxidation is inhibited by reduced pH in both surface and deep seawater (Huesemann et al., 2002). Conflicting results from the population/ecosystem and species levels indicate that community may play a crucial role in determining the response of microbes to OA. In addition to community structure and the number of species, micro-organism interaction is an important component of diversity (Olesen et al., 2007). For example, ecological networks among different species bridge ecosystem complexity and stability (Montoya et al., 2006). The interaction between plants and pollination enhances the relative resistance of plants to environmental disturbance (Sole and Montoya, 2001; Memmott et al., 2004). Compared with network investigations among macro-organisms (Elton, 1927; Paine, 1980; Bascompte et al., 2003), microbial interactions and ecological networks are understudied and have only been investigated recently with advances in molecular technology (Sherr and Sherr, 2008; Chaffron et al., 2010; Steele et al., 2011). Several microbial network investigations have been conducted on temporal variation in microbial communities and the interactions among bacteria, phage, and protists at the San Pedro Ocean Time-series (SPOT) station off southern California (Chow et al., 2013, 2014). Bacterial interaction has also been proposed as a determinant of phytoplankton bloom dynamics (Tan et al., 2015 (...truncated)