Effects of nutrient load on microbial activities within a seagrass-dominated ecosystem: Implications of changes in seagrass blue carbon

https://doi.org/10.1016/j.marpolbul.2017.01.056Get rights and content

Highlights

  • Responses of microbial activities to nutrient load were observed in seagrass meadows.

  • Bacterial and fungal biomass increased with elevated nutrient levels.

  • Nutrient load stimulated the extracellular enzyme activity related to carbon cycling.

  • Nutrient enrichment enhanced seagrass contribution to bacterial biomass.

  • Organic carbon sources of fungi appeared to be unaffected by nutrient loading.

Abstract

Nutrient loading is a leading cause of global seagrass decline, triggering shifts from seagrass- to macroalgal-dominance. Within seagrass meadows of Xincun Bay (South China Sea), we found that nutrient loading (due to fish farming) increased sediment microbial biomass and extracellular enzyme activity associated with carbon cycling (polyphenol oxidase, invertase and cellulase), with a corresponding decrease in percent sediment organic carbon (SOC), suggesting that nutrients primed microorganism and stimulated SOC remineralization. Surpisingly, however, the relative contribution of seagrass-derived carbon to bacteria (δ13Cbacteria) increased with nutrient loading, despite popular theory being that microbes switch to consuming macroalgae which are assumed to provide a more labile carbon source. Organic carbon sources of fungi were unaffected by nutrient loading. Overall, this study suggests that nutrient loading changes the relative contribution of seagrass and algal sources to SOC pools, boosting sediment microbial biomass and extracellular enzyme activity, thereby possibly changing seagrass blue carbon.

Introduction

Seagrass ecosystems are globally-significant hotspots for organic carbon (OC, ‘blue carbon’) sequestration and storage, estimated to store up to 19.9 Pt C in their sediments - an amount equivalent to 10–times that stored in the earth's terrestrial soils (Fourqurean et al., 2012, Duarte et al., 2013, Greiner et al., 2013, Macreadie et al., 2014). Sediment microorganisms have a prominent contribution in determining the balance between sediment organic carbon (SOC) storage and remineralization processes within seagrass meadows (Sparling, 1992, Chambers et al., 2016), and can also contribute to a significant proportion of the seagrass SOC (30% of living C and over 8% of total OC for surface sediments; Danovaro et al., 1994). The relative use of the different sources of OC (seagrass, macroalgae, epiphytes, microphytobenthos, terrestrial organic matter) by microbes living within seagrass sediment is thought to depend primarily on the lability of OC (Jones et al., 2003, Holmer et al., 2004). Microbes primarily stimulate important OC transformation through the release of carbon-cycling extracellular enzymes, which play an important role in all biogeochemical cycles as proximate agents in crucial processes such as OC decomposition and energy transfer (Karaca et al., 2011, Shao et al., 2015).

Seagrass beds have been declining rapidly at a rate of 7% per year (Waycott et al., 2009), mainly due to nutrient pollution (Green and Short, 2003, Green et al., 2015). Increased nutrient loads to coastal areas can trigger the overgrowth of algae, most commonly in the form of epiphytes and macroalgae within seagrass beds (Hauxwell and Valiela, 2004, Burkholder et al., 2007), causing increases in the relative contribution of algae to the SOC pool within seagrass meadows (Volkman et al., 2008, Macreadie et al., 2012). It is thought that bacteria switch from seagrass to algal OC sources due to algal OC generally being more labile (Holmer et al., 2004), and, consequently, algae materials have relatively lower carbon burial efficiencies than seagrasses (Cebrian, 1999, Banta et al., 2004). Indeed, López et al. (1998) found that the addition of nutrient to seagrass sediment significantly increased ammonification rates, microbial exo-enzymatic activities and enhanced decomposition of SOC. However, empirical evidence of distinct shifts in sediment microbial communities, enzyme production and microbial organic carbon sources within seagrass meadows in response to nutrient loading is otherwise rare.

In this study, we investigated how microbial processes influence SOC transformation in response to nutrient enrichment of a seagrass meadow. Our study site was a ~ 200 ha mixed seagrass meadow (dominated by Thalassia hemprichii) in the southern shallow waters of the Xincun Bay, South China Sea (Huang et al., 2006). Xincun Bay has a long-history of urbanization and industrial development (Fig. 1), which has put pressure on the seagrass meadow, including high nutrient loading originated from fish farm expansion (Zhang et al., 2014, Liu et al., 2016). Liu et al. (2016) reported that increased nutrient enrichment could enhance the relative contribution of seagrass and also macroalgae and epiphyte to SOC, causing elevation of SOC levels and microbial biomass in Xincun Bay. What we still don't know, however, is how microbial activities changes in response to shifts in SOC sources and composition induced by nutrient loading.

Here we assessed phospholipid fatty acid (PLFA) profiles (Bossio and Scow, 1998, Li et al., 2015, Chambers et al., 2016) and compound-specific stable carbon isotope of PLFA (Boschker et al., 2000, Abraham and Hesse, 2003, Jones et al., 2003, Holmer et al., 2004, Bouillon and Boschker, 2006, Kohl et al., 2015) to determine how microbial communities and the microbial OC sources change in response to nutrient enrichment. In addition, we investigated how the extracellular enzyme activities, including polyphenol oxidase, peroxidase, invertase and cellulase, influence OC decomposition (Waldrop et al., 2004, Yin et al., 2014, Li et al., 2015, Shao et al., 2015). Our goal was to generate empirical data that could help understand how nutrient loading affects the carbon-sink capacity of Xincun Bay, thereby aiding resource managers to better manage anthropogenic stressors that affect this nearly-closed bay.

Section snippets

Study site

Xincun Bay (18°24′34″N–18°24′42″N, 109°57′42″E–109°57′58″E) has only one narrow channel connecting to the South China Sea in the southwest (Fig. 2). T. hemprichii grows on sediment consisting of sand and terrigenous mud (Huang et al., 2006). In recent years, cage aquaculture has developed rapidly, and the nutrient concentration is more than twice higher at the seagrass bed nearest the fish farming area than at the farthest meadow, thereby providing a nutrient gradient along the seagrass meadow (

Seawater nutrient and sediment variables

The average concentrations of DIN and DIP in the seawater were 4.81 ± 2.18 μmol and 0.55 ± 0.38 μmol in the four times sampling, respectively (the first three seasons nutrient data come from Liu et al., 2016). Variations of DIN and DIP among the stations were shown in Fig. 3. There was significant difference in DIN concentrations among the three stations (p < 0.05), but not for DIP (p > 0.05). The DIN and DIP concentrations both showed a decreasing trend with increasing distance to the fish farming area.

Changes of organic carbon sources in sediment

The nutrient concentrations were generally higher in Xincun Bay than other seagrass beds reported in the literature (the DIN ranged from < 0.37 to 3.17 μM, and the DIP ranged from 0.06 to 0.64 μM; Ziegler and Benner, 1999, Ziegler et al., 2004, Kiswara et al., 2009, Apostolaki et al., 2010), indicative of high nutrient loading within the seagrass bed. Moreover, significantly higher nutrient concentrations of T. hemprichii tissue P contents and root N contents (Zhang et al., 2014), epiphytic algae

Conclusion

We found that higher nutrient loads to a seagrass meadow elevated the meadow's sediment microbial biomass, extracellular enzyme activities and the relative contribution of seagrass to bacteria, but considerably decreased F/B ratios compared to the low nutrient condition. These findings imply that high nutrient enrichment can enhance production of plant-derived OC to sediment, and thus increased microbes as well as its SOC transformation efficiency, which will presumably change seagrass blue

Acknowledgments

This research was supported by the National Basic Research Program of China (2015CB452905, 2015CB452902), the National Natural Science Foundation of China (nos. 41306108, 41406128), the National Specialized Project of Science and Technology (2015FY110600). PM was supported by an Australian Research Council DECRA Fellowship (DE130101084) and a Linkage Project (LP160100242).

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