Calcification acidifies the microenvironment of a benthic foraminifer (Ammonia sp.)

Calcareous foraminifera are well known for their CaCO3 shells. Yet, CaCO3 precipitation acidifies the calcifying fluid. Calcification without pH regulation would therefore rapidly create a negative feedback for CaCO3 precipitation. In unicellular organisms, like foraminifera, an effective mechanism to counteract this acidification could be the externalization of H+ from the site of calcification. In this study we showthat a benthic symbiont-free foraminifer Ammonia sp. actively decreases pH within its extracellular microenvironment only while precipitating calcite. During chamber formation events the strongest pH decreases occurred in the vicinity of a newly forming chamber (range of gradient ~100 μm) with a recorded minimum of 6.31 (b10 μm from the shell) and a maximumduration of 7 h. The acidification was actively regulated by the foraminifera and correlatedwith shell diameters, indicating that the amount of protons removed during calcification is directly related to the volume of calcite precipitated. The here presented findings imply that H+ expulsion as a result of calcification may be a wider strategy for maintaining pH homeostasis in unicellular calcifying organisms.

[1]  D. Lea Elemental and Isotopic Proxies of Past Ocean Temperatures , 2013 .

[2]  A. Telser Molecular Biology of the Cell, 4th Edition , 2002 .

[3]  Ulf Riebesell,et al.  Diffusion and reactions in the vicinity of plankton: A refined model for inorganic carbon transport , 1997 .

[4]  C. Brownlee,et al.  A Voltage-Gated H+ Channel Underlying pH Homeostasis in Calcifying Coccolithophores , 2011, PLoS biology.

[5]  H. Kitazato,et al.  Foraminifera promote calcification by elevating their intracellular pH , 2009, Proceedings of the National Academy of Sciences.

[6]  J. Erez,et al.  The role of seawater endocytosis in the biomineralization process in calcareous foraminifera , 2009, Proceedings of the National Academy of Sciences.

[7]  B. Jørgensen,et al.  Microelectrodes: Their Use in Microbial Ecology , 1986 .

[8]  V. Starczak,et al.  Influences of benthic boundary‐layer flow on feeding rates of ciliates and flagellates at the sediment‐water interface , 2001 .

[9]  M. Kühl,et al.  Microsensor studies of photosynthesis and respiration in larger symbiotic foraminifera. I The physico-chemical microenvironment of Marginopora vertebralis, Amphistegina lobifera and Amphisorus hemprichii , 2000 .

[10]  Jelle Bijma,et al.  Effect of seawater carbonate concentration on foraminiferal carbon and oxygen isotopes , 1997, Nature.

[11]  B. Jørgensen,et al.  Contribution of Chloroflexus respiration to oxygen cycling in a hypersaline microbial mat from Lake Chiprana, Spain. , 2007, Environmental microbiology.

[12]  Jelle Bijma,et al.  Model simulation of the carbonate chemistry in the microenvironment of symbiont bearing foraminifera , 1999 .

[13]  Ulf Riebesell,et al.  Species‐specific responses of calcifying algae to changing seawater carbonate chemistry , 2006 .

[14]  E. Rohling Paleosalinity: confidence limits and future applications , 2000 .

[15]  H. Elderfield,et al.  Planktonic foraminiferal Cd/Ca: Paleonutrients or paleotemperature? , 1999 .

[16]  J. Erez The Source of Ions for Biomineralization in Foraminifera and Their Implications for Paleoceanographic Proxies , 2003 .

[17]  G. Nehrke,et al.  Impact of seawater pCO2 on calcification and Mg/Ca and Sr/Ca ratios in benthic foraminifera calcite: results from culturing experiments with Ammonia tepida , 2010 .

[18]  M. Frenz,et al.  Coccolith contribution to South Atlantic carbonate sedimentation , 2004 .

[19]  M. Kühl,et al.  Microsensor studies of photosynthesis and respiration in the symbiotic foraminifer Orbulina universa , 1998 .

[20]  A. H. Compton,et al.  The Density of Rock Salt and Calcite , 1925 .

[21]  S. Grinstein,et al.  Proton conductance of the plasma membrane: properties, regulation, and functional role. , 1993, The American journal of physiology.

[22]  R. W. Angell Calcification during chamber development in Rosalina floridana , 1979 .

[23]  P. Martin,et al.  Calcium uptake and calcification rate in the planktonic foraminifer Orbulina universa , 1995 .

[24]  H. Hansen Shell construction in modern calcareous Foraminifera , 1999 .

[25]  H. Elderfield,et al.  Oceanic Cd/P ratio and nutrient utilization in the glacial Southern Ocean , 2000, Nature.

[26]  G. Nehrke,et al.  Physiological controls on seawater uptake and calcification in the benthic foraminifer Ammonia tepida , 2009 .

[27]  Hansen,et al.  ELECTRON MICROSCOPY OF ROTALIACEAN WALL STRUCTURES , 2009 .

[28]  A. E. Nielsen Kinetics of precipitation , 1964 .

[29]  N. Stambler,et al.  A microsensor study of light enhanced ca 2 + uptake and photosynthesis in the reef-building hermatypic coral , 2006 .

[30]  G. Gust,et al.  Impact of bioroughness on interfacia solute exchange in permeable sediments , 1992 .

[31]  K. Vickerman The diversity and ecological significance of Protozoa , 1992, Biodiversity & Conservation.

[32]  R. W. Angell The Test Structure and Composition of the Foraminifer Rosalina floridana , 1967 .

[33]  E. Padan,et al.  Mechanisms for the uptake of inorganic carbon by two species of symbiont-bearing foraminifera , 1989 .

[34]  J. Erez,et al.  The size and function of the internal inorganic carbon pool of the foraminifer Amphistegina lobifera , 1988 .

[35]  R. Zeebe,et al.  Comparison of two potential strategies of planktonic foraminifera for house building: Mg2+ or H+ removal? , 2002 .

[36]  C. Hemleben,et al.  Chamber Formation in Planktonic Foraminifera , 1979 .

[37]  D. Wolf-Gladrow,et al.  CO2 in Seawater: Equilibrium, Kinetics, Isotopes , 2001 .

[38]  I. Madshus,et al.  Regulation of intracellular pH in eukaryotic cells. , 1988, The Biochemical journal.

[39]  I. Probert,et al.  Calcification rate and temperature effects on Sr partitioning in coccoliths of multiple species of coccolithophorids in culture , 2002 .

[40]  S. Goldstein,et al.  Foraminifera: A biological overview , 1999 .

[41]  D. Lea 6.14 – Elemental and Isotopic Proxies of Past Ocean Temperatures , 2003 .

[42]  M. Kühl,et al.  The chemical microenvironment of the symbiotic planktonic foraminifer Orbulina universa , 2005 .

[43]  A. R. Loeblich,et al.  Foraminiferal evolution, diversification, and extinction , 1988 .

[44]  O. Anderson,et al.  An estimation of calcium carbonate deposition rate in a planktonic foraminifer Globigerinoides sacculifer using 45 Ca as a tracer; a recommended procedure for improved accuracy , 1984 .

[45]  C. A. Ross,et al.  Paleozoic Foraminifera. , 1991, Bio Systems.

[46]  Karl K. Turekian,et al.  Treatise on geochemistry , 2014 .

[47]  G. Nehrke,et al.  The impact of salinity on the Mg/Ca and Sr/Ca ratio in the benthic foraminifera Ammonia tepida: Results from culture experiments , 2010 .

[48]  J. Erez Calcification Rates, Photosynthesis and Light in Planktonic Foraminifera , 1983 .

[49]  P. Westbroek,et al.  Biomineralization and Biological Metal Accumulation , 1983 .

[50]  W. Simon,et al.  Intracellular neutral carrier-based Ca2+ microelectrode with subnanomolar detection limit , 1987, Pflügers Archiv.

[51]  C. You,et al.  Foraminiferal boron isotope ratios as a proxy for surface ocean pH over the past 21 Myr , 1993, Nature.