Biotic Control of Surface pH and Evidence of Light-Induced H+ Pumping and Ca2+-H+ Exchange in a Tropical Crustose Coralline Alga

Hofmann, Laurie C.; Koch, Marguerite S.; Beer, Dirk de

doi:10.1371/journal.pone.0159057

Cited by 51 publications

(89 citation statements)

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“…Our study demonstrates that northeast Altnatic rhodoliths contribute to this variability, as they 35 deviate from the typical trend of red macroalgae lacking or having inefficient CCMs. The high ∂ 13 C org signatures measured in our study support previous work suggesting that crustose coralline algae (CCA) can use HCO 3 -for calcification and photosynthesis (Comeau et al, 2013;Hofmann et al, 2016). Because CCA take up HCO 3 -for calcification (Comeau et al, 2013), the same transporters are likely used to supply inorganic carbon for photosynthesis, which would explain the high The linear relationship between skeletal ∂ 13 C signatures (∂ 13 C T ) and DIC observed in our study supports the notion that these signatures can be used as a proxy for seawater DIC in long-lived coralline algae (Williams et al, 2011).…”

Section: Discussionsupporting

confidence: 90%

Latitudinal trends in stable isotope signatures and carbon concentrating mechanisms of northeast Atlantic rhodoliths

Hofmann¹,

Heesch²

2017

Preprint

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Abstract. Rhodoliths are free-living calcifying red algae that form extensive beds in shallow marine benthic environments (< 250 m), which provide important habitats and nurseries for marine organisms and contribute to carbonate sediment accumulation. There is growing concern that these organisms are sensitive to global climate change, yet little is known about their physiology. Considering their broad distribution along most continental coastlines, their potential sensitivity to global 10 change could have important consequences for the productivity and diversity of benthic coastal environments. The goal of this study was to determine the plasticity of dissolved inorganic carbon (DIC) uptake mechanisms of rhodoliths along a latitudinal gradient in the Northeast (NE) Atlantic using natural stable isotope signatures. The δ 13 C signature of macroalgae can be used to provide an indication of the preferred inorganic carbon source (CO 2 vs. HCO 3 -). Here we present the total (δ 13 C T ) and organic (δ 13 C org ) δ 13 C signatures of NE Atlantic rhodoliths with respect to changing environmental conditions 15 along a latitudinal gradient from the Canary Islands to Spitsbergen. The δ 13 C T signatures (-11.9 to -0.89) of rhodoliths analysed in this study were generally higher than the δ 13 C org signatures, which ranged from -25.7 to -2.8. We observed a decreasing trend in δ 13 C T signatures with increasing latitude and temperature, while δ 13 C org signatures were only significantly correlated to DIC. These data suggest that high latitude rhodoliths rely solely on CO 2 as an inorganic carbon source, while low latitudes rhodoliths likely take up HCO 3 -directly. However, depth also has a significant effect on both skeletal and 20 organic δ 13 C signatures, suggesting that both local and latitudinal trends influence the plasticity of rhodolith inorganic carbon acquisition and assimilation. Our results show that many species, particularly those at lower latitudes, have carbon concentrating mechanisms that facilitate HCO 3 -use for photosynthesis. This is an important adaptation for marine macroalgae, because HCO 3 -is available at higher concentrations than CO 2 in seawater, and this becomes even more extreme with increasing temperature. The flexibility of CCMs in northeast Atlantic rhodoliths observed in our study may provide a 25 key physiological mechanism for potential adaptation of rhodoliths to future global climate change.

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Section: Discussionsupporting

confidence: 90%

Latitudinal trends in stable isotope signatures and carbon concentrating mechanisms of northeast Atlantic rhodoliths

Hofmann¹,

Heesch²

2017

Preprint

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“…Net production in light and respiration in dark conditions were defined as interfacial oxygen fluxes (Hofmann et al., ), calculated from the raw concentration values of the profiles using Fick's first law (Revsbech & Jørgensen, ):

J = - D (\frac{normald c}{normald x}),

with J : interfacial oxygen fluxes in μmol O 2 m −2 s −1 , D : diffusion coefficient of oxygen in seawater in m 2 /s ( D = 1.66 × 10 −9 at 13.2°C and salinity 37, value calculated with the r package marelac), d c : the change in concentration in the DBL in μmol/m 3 and d x : the thickness of the DBL in m .…”

Section: Methodsmentioning

confidence: 99%

“…In this thin laminar layer, movement of ions and molecules is by molecular diffusion, and the metabolic activity of the organism results in a concentration gradient due to the uptake and release of dissolved substances to and from the organism's surface (Hurd, ; Vogel, ). Fluctuations observed in these microhabitats at the surface of seaweed are mainly driven by their photosynthesis and respiration processes under the control of light (Cornwall, Hepburn, Pilditch, & Hurd, ; Hofmann, Koch, & de Beer, ; Hurd et al., ; Sand‐Jensen, Revsbech, & Jörgensen, ). Thus, metabolic activity affects the microchemical environment of the DBL which differs from that in the mainstream seawater just micrometres away (Hurd, ), with implications for the alga itself and all the other small organisms living on the blades.…”

Section: Introductionmentioning

confidence: 99%

Abiotic and biotic interactions in the diffusive boundary layer of kelp blades create a potential refuge from ocean acidification

Noisette

Hurd

2018

Functional Ecology

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Seaweeds are able to modify the chemical environment at their surface, in a micro‐zone called the diffusive boundary layer (DBL), via their metabolic processes controlled by light intensity. Depending on the thickness of the DBL, sessile invertebrates such as calcifying bryozoans or tube‐forming polychaetes living on the surface of the blades can be affected by the chemical variations occurring in this microlayer. Especially in the context of ocean acidification (OA), these microhabitats might be considered as a refuge from lower pH, because during the day photosynthesis temporarily raises the pH to values higher than in the mainstream seawater. We assessed the thickness and the characteristics of the DBL at two pH levels (today's average surface ocean pH 8.1 and a reduced pH predicted for the end of the century, pH 7.7) and seawater flows (slow, 0.5 and fast, >8 cm/s) on Ecklonia radiata (kelp) blades. Oxygen and pH profiles from the blade surface to the mainstream seawater were measured with O2 and pH microsensors for both bare blades and blades colonized by the bryozoan Membranipora membranacea. The DBL was thicker in slow flow compared with fast flow and the presence of bryozoans increased the DBL thickness and shaped the DBL gradient in dark conditions. Net production was increased in the low pH condition, increasing the amount of oxygen in the DBL in both bare and epiphytized blades. This increase drove the daily pH fluctuations at the blade surface, shifting them towards higher values compared with today's pH. The presence of bryozoans led to lower oxygen concentrations in the DBL and more complex pH fluctuations at the blade surface, particularly at pH 7.7. Overall, this study, based on microprofiles, shows that, in slow flow, DBL microenvironments at the surface of the kelps may constitute a refuge from OA with pH values higher than those of the mainstream seawater. For calcifying organisms, it could also represent training ground for harsh conditions, with broad daily pH and oxygen fluctuations. These chemical microenvironments, biologically shaped by the macrophytes, are of great interest for the resilience of coastal ecosystems in the context of global change. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13067/suppinfo is available for this article.

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“…Seawater in the pH manipulated enclosure was lower than ambient yet, it remained 469 saturated with respect to both calcite and aragonite (3.6 and 2.2). CCA have the ability to raise 470 the pH within their boundary layer to limit the potential negative impacts of decreased ambient 471 pH when seawater is not undersaturated (Hofmann et al 2016). In contrast, at CO2 seeps, pH 472 near the vents can be highly variable and organisms can be exposed to pH levels substantially 473 lower than projections for the next century (Kerrison et al 2011).…”

Section: Mineralogy 334mentioning

confidence: 99%

Effects of in situ CO2 enrichment on Posidonia oceanica epiphytic community composition and mineralogy

et al. 2017

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Alterations in seagrass epiphytic communities are expected under future ocean 21 acidification conditions, yet this hypothesis has been little tested in situ. A Free Ocean Carbon 22Dioxide Enrichment (FOCE) system was used to lower pH by a ~ 0.3 unit offset within a 23 partially enclosed portion (1.7 m 3 ) of a Posidonia oceanica meadow (11 m depth) between 21 24June and 3 November 2014. Leaf epiphytic community composition (% cover) and bulk 25 epiphytic mineralogy were compared every four weeks within three treatments, located in the 26 same meadow: a pH-manipulated (experimental enclosure) and a control enclosure, as well as a 27 nearby ambient area. Percent coverage of invertebrate calcifiers and crustose coralline algae 28 (CCA) did not appear to be affected by the lowered pH. Furthermore, fleshy algae did not 29 proliferate at lowered pH. Only Foraminifera, which covered less than 3% of leaf surfaces, 30 declined in manner consistent with ocean acidification predictions. Bulk epiphytic magnesium 31 carbonate composition was similar between treatments and percentage of magnesium appeared 32 2 to increase from summer to autumn. CCA did not exhibit any visible skeleton dissolution or 33 mineral alteration at lowered pH and carbonate saturation state. Negative impacts from ocean 34 acidification on P. oceanica epiphytic communities were smaller than expected. Epiphytic 35 calcifiers were possibly protected from the pH treatment due to host plant photosynthesis inside 36 the enclosure where water flow is slowed. The more positive outcome than expected suggests 37 that calcareous members of epiphytic communities may find refuge in some conditions and be 38

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Biotic Control of Surface pH and Evidence of Light-Induced H+ Pumping and Ca2+-H+ Exchange in a Tropical Crustose Coralline Alga

Cited by 51 publications

References 67 publications

Latitudinal trends in stable isotope signatures and carbon concentrating mechanisms of northeast Atlantic rhodoliths

Latitudinal trends in stable isotope signatures and carbon concentrating mechanisms of northeast Atlantic rhodoliths

Abiotic and biotic interactions in the diffusive boundary layer of kelp blades create a potential refuge from ocean acidification

Effects of in situ CO2 enrichment on Posidonia oceanica epiphytic community composition and mineralogy

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