Elsevier

Science of The Total Environment

Volume 686, 10 October 2019, Pages 264-275
Science of The Total Environment

Vulnerability of seagrass blue carbon to microbial attack following exposure to warming and oxygen

https://doi.org/10.1016/j.scitotenv.2019.05.462Get rights and content

Highlights

  • Seagrass ecosystems store globally-significant amounts of blue carbon

  • Mechanisms underpinning blue carbon destabilisation are largely unknown

  • Exposure of blue carbon to oxygen triggered microbial remineralization

  • Sediment carbon turnover increased 34–38-fold following oxygen exposure

  • Activities that expose seagrass sediments to oxygen threaten blue carbon stability

Abstract

Seagrass meadows store globally-significant quantities of organic ‘blue’ carbon. These blue carbon stocks are potentially vulnerable to anthropogenic stressors (e.g. coastal development, climate change). Here, we tested the impact of oxygen exposure and warming (major consequences of human disturbance) on rates of microbial carbon break-down in seagrass sediments. Active microbes occurred throughout seagrass sediment profiles, but deep, ancient sediments (~5000 yrs. old) contained only 3% of the abundance of active microbes as young, surface sediments (<2 yrs. old). Metagenomic analysis revealed that microbial community structure and function changed with depth, with a shift from proteobacteria and high levels of genes involved in sulfur cycling in the near surface samples, to a higher proportion of firmicutes and euraracheota and genes involved in methanogenesis at depth. Ancient carbon consisted almost entirely (97%) of carbon considered ‘thermally recalcitrant’, and therefore presumably inaccessible to microbial attack. Experimental warming had little impact on carbon; however, exposure of ancient sediments to oxygen increased microbial abundance, carbon uptake and sediment carbon turnover (34–38 fold). Overall, this study provides detailed characterization of seagrass blue carbon (chemical stability, age, associated microbes) and suggests that environmental disturbances that expose coastal sediments to oxygen (e.g. dredging) have the capacity to diminish seagrass sediment carbon stocks by facilitating microbial remineralisation.

Introduction

‘Blue carbon’ ecosystems, which include seagrass meadows, tidal marshes and mangrove forests, hold large reservoirs of organic carbon (McLeod et al., 2011). Despite occupying <1% of the seafloor, blue carbon ecosystems contribute half of all organic carbon (OC) sequestered through burial in the oceans (Duarte et al., 2013). Blue carbon ecosystems have the ability to capture CO2-OC in soil, where it can remain locked away for millennia; thereby acting as natural sinks of carbon, effectively reducing atmospheric CO2 concentrations that contribute to global warming (McLeod et al., 2011). The disproportionally large influence of blue carbon ecosystems on the global carbon cycle means that altering the stock of carbon in their soils will likely influence global greenhouse gas budgets.

Despite the impact of blue carbon, we know very little about the mechanisms responsible for the retention of carbon in blue carbon environments. For example, when existing blue carbon ecosystems are disturbed (e.g. via coastal development, climate change), little is known to what extent is stored OC broken down and released into the atmosphere, and whether this varies in response to environmental and edaphic conditions, or when management actions result in new lands coming under tidal influence at what rate is carbon sequestered. Knowledge of these mechanisms is critical in understanding the dynamics of blue carbon cycling and informing such conservation management issues as: identifying coasts under threat of blue carbon loss, quantifying the impact/outcomes of blue carbon loss, identifying where enhanced blue carbon sequestration may be possible and developing blue carbon markets. Due to lack of robust data on the fate of blue carbon following disturbance, the scientific community has relied on risk assessment approaches and expert solicitation until this knowledge gap is filled (Lovelock et al., 2017).

A key aspect in the success of blue carbon ecosystems as natural carbon sinks is their ability to accumulate OC that resists or evades microbial attack (Macreadie et al., 2017). Microbes control key biogeochemical pathways, therefore changes in microbial activity and community structure could affect the stability of blue carbon (Kearns et al., 2016). According to the terrestrial soil literature, which is much more advanced in its understanding of the mechanisms underpinning the stabilisation or destabilisation of OC (Sollins et al., 1996), there are four key pathways in which carbon might remain preserved within blue carbon environments and evade breakdown (remineralisation) by microbes: intrinsic chemical stability (Baldock et al., 2004); physical mechanisms of protection (e.g. adsorption or binding to minerals) (Torn et al., 1997); the absence of in situ microbial communities with the capacity to produce enzymes for degradation to occur (Arnosti, 2004); and environmental conditions hostile to microbial activity (Bianchi, 2011). Much research effort has focused on intrinsic chemical stability, mostly from the terrestrial soil literature (Kleber, 2010; Kleber et al., 2011), but also more recently from marine environments (Trevathan-Tackett et al., 2015; Trevathan-Tackett et al., 2017a), where OC is often viewed on a spectrum of susceptibility to microbial attack, ranging from ‘labile’ OC, that has high susceptibility to microbial attack, to ‘recalcitrant’ OC, which has low susceptibility to microbial attack.

We focus on seagrass meadows, because they are thought to be facing a ‘global crisis’ (Orth et al., 2006), putting at risk up to 299 million tons OC yr−1 (Fourqurean et al., 2012). Warmer waters and oxygen exposure of seagrass sediments have already been implicated as causes of loss of blue carbon from seagrass ecosystems (e.g. Arias-Ortiz et al., 2018; Macreadie et al., 2015), but as yet our understanding of the microbial processes and mechanisms behind the observed responses is very limited and have been identified as an urgent knowledge gap for seagrass ecosystem management (Belshe et al., 2017; Macreadie et al., 2014; Trevathan-Tackett et al., 2017c). Furthermore, there have been conflicting results. For example, while some studies report increased OC remineralization due to warming (Pedersen et al., 2011), others have reported no effect. It is generally agreed that disturbances (e.g. via eutrophication, dredging, coastal development, climate change) to seagrass and other blue carbon ecosystems cause losses of OC (Macreadie et al., 2013), but what's not clear is whether the OC becomes remineralised by microbes and converted into atmospheric CO2, or whether the OC is simply exported elsewhere and re-buried? The answer to this question is crucial for global seagrass OC budgets.

Our overarching aim of this study was to gain understanding of how blue carbon recalcitrance is achieved and the risk of seagrass blue carbon becoming destabilized in response to biotic and environmental change. More specifically, our objectives were to: 1) Characterise recalcitrant blue carbon from seagrass meadows; 2) Characterise the functional capacity of microbial communities associated with recalcitrant blue carbon from seagrass meadows; and 3) Quantify the importance of environmental controls (oxygen exposure and warming) over seagrass blue carbon recalcitrance.

Section snippets

Materials and methods

We sought to understand which of the key pathways in Table 1 may be responsible (whole or in part) for blue carbon preservation in seagrass meadows. To achieve this we performed a series of surveys and experiments to infer and test the potential vulnerability of seagrass OC to disturbance, specifically temperature increases and oxygen exposure. Warming and oxygen were selected because they are among the most common and widespread forms of disturbances to seagrass meadows; warming due to climate

Characterising a seagrass blue carbon core: Stocks, provenance, and rates of accumulation

The seagrass sediments used in this research spanned a period of 5000 years, according to 210Pb and radiocarbon (14C) dating (Fig. 2, Table S1). Surface sediment ages were 1.7 ± 1.3 years in the top 0–0.5 cm, reaching 84.8 ± 15.1 years in the 4–4.5 cm (Fig. 2, Table S1), with a mass accumulation rate of 0.112 g cm−1 yr−1 over this depth. The down-core average of the proportion of OC was 1.66 ± 0.77% (Fig. 2), which is lower than the global average for seagrass of 2.5 ± 0.1% (Fourqurean et al.,

Summary and conclusions

As the coastal zone faces increasing anthropogenic pressure, it is important to understand whether blue carbon reservoirs are at risk of being remineralised by microbes and released to the atmosphere as CO2 or other greenhouse gases. Here, we characterized blue carbon sediment profiles from seagrass meadows and then tested the vulnerability of blue carbon to oxygen exposure and warming. Sediment profiles spanned a period from the present day to ~5000 years old. Flow cytometric analysis showed

Funding

We acknowledge the support of an Australian Research Council (ARC) Discovery Early Career Researcher Award DE130101084 (PM), an ARC Linkage Grant LP160100242 (PM), the CSIRO Coastal Carbon Cluster (PM, TA, JS, RC), and an ARC Future Fellowship FT130100218 (JS).

Author contributions

PM conceived the idea. PM, TA, JS, MSF, JS and DA carried out the experiments and analyses. All authors contributed to writing the manuscript. The authors declare no competing interests.

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