Strong leaf surface basification and CO₂limitation of seagrass induced by epiphytic biofilm microenvironments

Abstract

Coastal eutrophication is a growing problem worldwide, leading to increased epiphyte overgrowth of seagrass leaves. Yet little is known about how epiphytes affect key biogeochemical conditions and processes in the seagrass phyllosphere. We used electrochemical microsensors to measure microgradients of O2, pH, and CO2 at the bare and epiphyte‐covered leaf surface of seagrass (Zostera marina L.) to determine effects of epiphytes on the leaf chemical microenvironment. Epiphytes result in extreme daily fluctuations in pH, O2, and inorganic carbon concentrations at the seagrass leaf surface severely hampering the plant's performance. In light, leaf epiphyte biofilms and their diffusive boundary layer lead to strong basification, markedly reducing the CO2 and HCO3‐ availability at the leaf surface, leading to reduced photosynthetic efficiency as a result of carbon limitation and enhanced photorespiration. With epiphytes, leaf surface pH increased to >10, thereby exceeding final pH levels (~9.62) and CO2 compensation points for active photosynthesis. In darkness, epiphyte biofilms resulted in increased CO2 and hypoxia at the leaf surface. Epiphytes can lead to severe carbon limitation in seagrasses owing to strong phyllosphere basification leading to CO2 depletion and costly, yet limiting, HCO3‐ utilization, increasing the risk of plant starvation.

Imaging O2 dynamics and microenvironments in the seagrass leaf phyllosphere with magnetic optical sensor nanoparticles

“…TDDs of 500-1200 µm; Figure S4) impeding gas exchange with the surrounding water (Jørgensen and Revsbech, 1985;Hurd, 2000). This O 2 build-up in the leaf microenvironment can have severe negative effects on the photosynthetic efficiency of a leaf through increased photorespiration (Brodersen et al, 2015a(Brodersen et al, , 2020Kim et al, 2018;Larkum et al, 2018), as a result of increased oxygenation of ribulose 1,5-bisphosphate (RuBP), leading to reduced RuBP carboxylase-to-oxygenase activity (Beer and Rehnberg, 1997;Beer et al, 2002), and thus reduced CO 2 fixation by RuBisCO.…”

“…Coastal eutrophication leads to increased epiphytic biofilm overgrowth on seagrass leaves (Borum, 1985), which shades the leaves from vital light (Brodersen et al, 2015a) and restricts gas and nutrient exchange with the surrounding environment (Brodersen et al, 2015a(Brodersen et al, , 2020. Sufficient internal plant aeration is essential for healthy seagrasses, as the seagrass below-ground tissue grow in a largely anoxic sediment environment (Frederiksen and Glud, 2006;Brodersen et al, 2017a).…”

“…Sufficient internal plant aeration is essential for healthy seagrasses, as the seagrass below-ground tissue grow in a largely anoxic sediment environment (Frederiksen and Glud, 2006;Brodersen et al, 2017a). Reduced water-column O 2 conditions at night (Greve et al, 2003;Borum et al, 2005) as well as thick epiphytic biofilms lead to reduced internal plant aeration (Pedersen et al, 2004;Brodersen et al, 2015aBrodersen et al, , 2020, which increases the risk of suffocation.…”

“…The O 2 supply to the above-and below-ground tissues of seagrass is thus largely determined by the leaf microenvironment, where epiphytic biofilms: (i) reduce and alter the spectral composition of light reaching the leaves during the day (Brodersen et al, 2015a); and (ii) compete for the available O 2 passively diffusing into the leaf microenvironment from the surrounding water column at night (Brodersen et al, 2015a(Brodersen et al, , 2020. Detailed 1-dimensional (1D) microsensor measurements across the epiphytic biofilm to the leaf surface have revealed that the overall leaf physicochemical microenvironment frequently alters from being supersaturated in the day to being hypoxic at night (Brodersen et al, 2015a;Kim et al, 2018;Larkum et al, 2018), as a result of light-driven photosynthesis and respiration processes, respectively.…”

“…The TDD determines the strength of the inward and outward diffusion resistance for gases and solutes (Larkum et al, 1989(Larkum et al, , 2006b. Epiphytic biofilms can thus lead to dynamic oxic or hypoxic/anoxic microniches within the seagrass phyllosphere, where a thick and dense epiphytic biofilm may lead to local supersaturation in light and anoxia in darkness (Brodersen et al, 2020).…”