Fresh carbon inputs to seagrass sediments induce variable microbial priming responses

Highlights

• Microbial priming is a potential mechanism for remineralization of carbon (C) stocks to CO₂.

• CO₂ emissions were measured from sediments exposed to fresh C and disturbance

• Priming resulted in a 2–3-fold increase in CO₂ released from sediment C compared to control

• Priming is likely a greater threat to deep C stocks undergoing physical disturbance

Abstract

Microbes are the ‘gatekeepers’ of the marine carbon cycle, yet the mechanisms for how microbial metabolism drives carbon sequestration in coastal ecosystems are still being defined. The proximity of coastal habitats to runoff and disturbance creates ideal conditions for microbial priming, i.e., the enhanced remineralisation of stored carbon in response to fresh substrate availability and oxygen introduction. Microbial priming, therefore, poses a risk for enhanced CO₂ release in these carbon sequestration hotspots. Here we quantified the existence of priming in seagrass sediments and showed that the addition of fresh carbon stimulated a 1.7- to 2.7-fold increase in CO₂ release from recent and accumulated carbon deposits. We propose that priming taking place at the sediment surface is a natural occurrence and can be minimised by the recalcitrant components of the fresh inputs (i.e., lignocellulose) and by reduced metabolism in low oxygen and high burial rate conditions. Conversely, priming of deep sediments after the reintroduction to the water column through physical disturbances (e.g., dredging, boat scars) would cause rapid remineralisation of previously preserved carbon. Microbial priming is identified as a process that weakens sediment carbon storage capacity and is a pathway to CO₂ release in disturbed or degraded seagrass ecosystems; however, increased management and restoration practices can reduce these anthropogenic disturbances and enhance carbon sequestration capacity.

Introduction

Vegetated coastal ecosystems, including seagrasses, mangroves and saltmarshes, have a disproportionately large influence on ocean carbon sequestration considering their relatively small (0.1%) footprint on the seafloor (Duarte et al., 2013, McLeod et al., 2011). For this reason, coastal ecosystems are at the forefront of research aimed at using these ecosystems to offset atmospheric CO₂ through the natural process of ‘biosequestration’ (Macreadie et al., 2017). Microbial metabolism ultimately determines how much organic carbon is sequestered and stored or returned to the atmosphere (Arnosti, 2011, Burd et al., 2016). The accumulation of organic carbon (OC) deposits is enhanced in predominantly anoxic and low-nutrient conditions that limit microbial remineralisation rates (Burdige, 2007) – conditions characteristic of vegetated coastal habitats. Despite these ideal characteristics for long-term carbon accumulation and preservation in vegetated coastal habitats, these ecosystems have been challenged by high rates of habitat degradation and losses in recent decades, much of which has been attributed to anthropogenic activities, such as nutrient and organic matter runoff and physical disturbances (Hopkinson et al., 2012, Orth et al., 2006, Serrano et al., 2016, Waycott et al., 2009). Habitat destruction not only diminishes the sediment organic carbon (SOC)-accumulation capacity of vegetated coastal habitats (Macreadie et al., 2012), but increases the risk of losing existing SOC (Fourqurean et al., 2012, Graca et al., 2004, Macreadie et al., 2015, Marbà et al., 2015).

The combination of fresh OC inputs and physical disturbances of deep SOC also creates ideal conditions for exacerbated SOC loss via the stimulation of microbial remineralisation, i.e., the ‘microbial priming effect’. The priming effect is a phenomenon in which a disturbance or access to fresh, organic carbon (OC, e.g. priming source) or inorganic nutrients stimulates microbes to metabolise SOC that would not have been otherwise utilised or would have been utilised at considerably slower rates (Kuzyakov et al., 2000). This concept is widely accepted for terrestrial soil ecosystems and marine pelagic and seafloor sediments, and has been shown in some instances to more than double the amount of soil or sediment OC metabolised by microbes (Bianchi, 2011, Fontaine et al., 2007, Guenet et al., 2010, van Nugteren et al., 2009), Yet, microbial priming has yet to be directly quantified in coastal vegetated ecosystems.

The microbial priming effect is likely to pose a significant threat to net SOC loss and CO₂ release within marine or coastal ecosystems via (1) the injection of fresh OC into deep sediments by bioturbation (Kristensen et al., 2011); (2) the addition of inorganic nutrients causing changes to porewater dynamics and bacterial nutrient limitations (López et al., 1998); and (3) the displacement of deep sediments (Kuzyakov et al., 2000) to the water column or sediment surface (and fresh nutrients or OC) via physical disturbances like dredging and boating activities. The addition of fresh OC in the form of microalgae or seagrass detritus has been shown to increase bacterial respiration and biomass in coastal sediments (Danovaro et al., 1994, Farjalla et al., 2009), indicating the potential for enhanced SOC remineralisation. Since the quality of the priming source provided to microbes by microalgae and seagrass detritus produces differential microbial remineralisation patterns (Enríquez et al., 1993) and microbial communities (Trevathan-Tackett et al., 2017b), different types of priming sources could likewise induce different degrees of priming.

This study quantified the existence of the microbial priming effect in coastal seagrass sediments and revealed its potential role in weakening seagrass SOC stocks. We added two common, natural priming sources: microalgae (Chlorella) to represent an algae bloom and Zostera muelleri seagrass to represent leaf inputs during senescence. Both priming sources were enriched with ¹³C before adding them to the sediments from two depths in order to simulate undisturbed (surface) and disturbed (deep) sediments. To assess the microbial priming effect, we quantified the amount of CO₂ respired after fresh OC additions in comparison to controls. Using the enriched isotope signatures, we also traced the OC source (priming source or SOC) being metabolised by microbes by analysing δ¹³C values of CO₂. We hypothesised that the addition of both forms of fresh OC will induce a priming effect, but microalgal OC would be utilised more rapidly than detrital seagrass OC due to higher relative lability. We also hypothesise that since total OC typically decreases with sediment depth that surface sediments may produce a larger priming effect due to a higher existing SOC content available for remineralisation.