Biogeochemical drivers of phosphatase activity in salt marsh sediments

Highlights

• The acidic sediment pH favors acid phosphatase activity.

• Humic acids influence phosphorus cycling due to inhibition of phosphatase activity.

• Higher phosphatase activity leads to higher inorganic phosphorous levels.

• Phosphatases are very important in phosphorus cycling and thus to primary producers metabolism.

Abstract

Although nitrogen has become a major concern for wetlands scientists dealing with eutrophication problems, phosphorous represents another key element, and consequently its biogeochemical cycling has a crucial role in eutrophication processes. Microbial communities are a central component in trophic dynamics and biogeochemical processes on coastal systems, since most of the processes in sediments are microbial-mediated due to enzymatic action, including the mineralization of organic phosphorus carried out by acid phosphatase activity. In the present work, the authors investigate the biogeochemical sediment drivers that control phosphatase activities. Authors also aim to assess biogeochemical factors' influence on the enzyme-mediated phosphorous cycling processes in salt marshes. Plant rhizosediments and bare sediments were collected and biogeochemical features, including phosphatase activities, inorganic and organic phosphorus contents, humic acids content and pH, were assessed. Acid phosphatase was found to give the highest contribution for total phosphatase activity among the three pH-isoforms present in salt marsh sediments, favored by acid pH in colonized sediments. Humic acids also appear to have an important role inhibiting phosphatase activity. A clear relation of phosphatase activity and inorganic phosphorous was also found. The data presented reinforces the role of phosphatase in phosphorous cycling.

Introduction

Salt marshes are highly productive areas located in the interface between freshwater and marine systems, often subjected to high nutrient loadings due to anthropogenic activity that can lead to systems eutrophication (Tobias et al., 2001). Salt marshes have been regarded as intertidal wastelands, but currently their important role in coastal defense, as a biodiversity pool, as nursing, shelter and feeding areas for several animals and as a source of organic materials and nutrients for marine communities is widely recognized (Boorman, 1999).

Another important function of salt marshes is their role as a sink of pollutants like heavy metals or excess nutrients. Conversely, salt marshes could also become a source of pollutants due to exportation of dead biomass, although the amount of contaminants exported is lower than the amount of contaminants retained (Caçador et al., 2009, Duarte et al., 2008).

Excess nutrients such as nitrogen (N) and phosphorus (P) can have damaging effects, leading to eutrophication of coastal waters (Andrieux-Loyer et al., 2008; Howarth et al., 2011). Although nitrogen is considered to be a major concern when dealing with eutrophication, phosphorus is also considered to be one of the key limiting nutrients to primary productivity and therefore it is one of the nutrients responsible for eutrophication (Correl, 1998, Paerl, 2009). Phosphorous is delivered to aquatic systems in several forms such as longer chain poly-phosphates, pyrophosphates, organic phosphate esters and phosphodiesters, and organic phosphonates. This element may also be delivered both in the dissolved and particulated form being deposited in the salt marsh sediments (Correl, 1998). However, P is only biologically available when it is in the inorganic form, as orthophosphate.

Sediment microbial communities are an essential component in trophic dynamics and biogeochemical processes in coastal ecosystems. The microbial community synthesizes extracellular enzymes that are responsible for the decomposition processes. Phosphatases are extracellular hydrolases that catalyze the mineralization of organic phosphorus into inorganic and more easily metabolized forms of phosphorus. One large and important group of these enzymes are the phosphomonoesterases and their pH-isoforms: alkaline, acid and neutral phosphatases, being therefore active in several kinds of sediments (Alef et al., 1998).

Although phosphatases are not exclusively produced by the microflora (being also produced as exudates by plant roots), microbial growth is favored by salt marsh plants that release oxygen from the root system into the sediments promoting reactions with reduced species (Caetano et al., 2011, Lillebø et al., 2006). In fact, Spartina maritima marshes have been shown to have an important role on phosphorus bioavailability decreasing total P, probably due to uptake for growth purposes (Lillebø et al., 2007). Also, due to the release of oxygen by plant root systems into the sediment, P efflux is reduced (Lillebø et al., 2007). Plant roots can also affect microbial communities due to root exudates input to the rhizosphere (Hartman et al., 2009). Plant type has also been shown to alter microbial community structure and function affecting microbial activity (Garbeva et al., 2008).

Due to the elevation gradient from the upland marsh to the lower mudflats, a physic-chemical gradient is generated allowing the colonization by different halophytic species (Halimione portulacoides, Sarcocornia fruticosa, Sarcocornia perennis and S. maritima) providing differential cycling areas along the marsh. This way, in the present work the authors aim to clarify the influence of the biogeochemical marsh environment on the activity extracellular phosphatases and thus how this modulates the phosphorous recycling in marsh sediments.