mineral brucite [Mg(OH)2]; minor amounts of magnesite and calcite were also detected. We propose that cell infill may be associated with the development of ...
J. Phycol. 51, 403–407 (2015) © 2015 Phycological Society of America DOI: 10.1111/jpy.12299
LETTER DISCOVERY OF THE MINERAL BRUCITE (MAGNESIUM HYDROXIDE) IN THE TROPICAL CALCIFYING ALGA POLYSTRATA DURA (PEYSSONNELIALES, RHODOPHYTA) Merinda C. Nash, Bayden D. Russell, Kyatt R. Dixon, Minglu Liu and Huifang Xu Red algae of the family Peyssonneliaceae typically form thin crusts impregnated with aragonite. Here, we report the first discovery of brucite in a thick red algal crust (~1 cm) formed by the peyssonnelioid species Polystrata dura from Papua New Guinea. Cells of P. dura were found to be infilled by the magnesium-rich mineral brucite [Mg(OH)2]; minor amounts of magnesite and calcite were also detected. We propose that cell infill may be associated with the development of thick (> ~5 mm) calcified red algal crusts, integral components of tropical biotic reefs. If brucite infill within the P. dura crust enhances resistance to dissolution similarly to crustose coralline algae that infill with dolomite, then these crusts would be more resilient to future ocean acidification than crusts without infill.
Peyssonnelia are a genera of red algae in the family Peyssonneliaceae. Peyssonnelia may be calcified or uncalcified (Krayesky et al. 2009). The extent and pattern of calcium carbonate (CaCO3) deposition in members of the Peyssonneliales varies greatly among taxa, forming within the thallus, or as an external layer beneath the basal most cell layer (hypobasal calcification), or both (Denizot 1968). Despite the varying nature of the calcification, it is widely thought that aragonite is the only phase of CaCO3 present in species of Peyssonneliales (James et al. 1988, Womersley 1994, Bilan and Usov 2001, Pueschel and Saunders 2009). Surveys were conducted to sample the calcifying algae growing around natural CO2 vents and control sites at Milne Bay, Papua New Guinea (Fabricius et al. 2011). Thirteen peyssonnelioid samples were collected from the control site (n = 9) and the CO2 vent site (n = 4). The thickest crust (1 cm) was from the control site encrusting on a coral (Fig. 1A) and was identified as belonging to the genus Polystrata Heydrich (Peyssonneliaceae). The other samples were not identified to species. This thick crust overgrowing a coral branch was considered
unusual as typically coralline algae (not peyssonnelioids) form thick crusts over coral substrate (Basso 2012). Further, coralline algae form their crusts with the carbonate Mg-calcite, whereas the Peyssonneliaceae reportedly deposit only aragonite. Peyssonnelioid samples were collected in April 2011 at 4–6 m depth using SCUBA, by breaking crusts from the reef surface using a dive knife. Samples were air-dried. The thick crust from which we report the presence of brucite was collected at the Dobu control site and has been deposited at the Connell Memorial Herbarium (UNB; collection number GWS036244). This crust exhibited a morphology and internal anatomy consistent with the original description of Polystrata dura (Heydrich 1905), and subsequent observations (Kato et al. 2006, Basso 2012), most notably a thick crust composed of numerous closely appressed overgrowing blades (Fig. 1B), each with a thin, monostromatic ventral perithallus (Fig. 1C) and heavy internal calcification (Fig. 1D), but lacking hypobasal calcification. Repeated attempts to amplify several genetic markers for molecular identification failed, presumably due to degradation of the DNA. 403
The matching anatomical features and proximity of the collection site to the type locality of P. dura, also in Papua New Guinea, were deemed adequate for species identification. For powder X-ray diffraction (XRD), a subsample, which included carbonate from the top growth layer to the base of the crust, was broken off and analyzed. XRD methods followed Nash et al. (2013a). Scanning electron microscopy–electron dispersive spectroscopy (SEM-EDS) was carried out at the Centre for Advanced Microscopy at the Australian National University. For these analyses, we used a Zeiss UltraPlus field emission scanning electron microscope equipped with an HKL electron backscatter diffraction operated at 15 kV, 11 mm working distance. The alga was mounted using carbon tape and was carbon-coated prior to microscopy but was not polished. Following these analyses, the exact piece used for SEM was sent for micro-XRD analysis. The 100-lm beam allows XRD analysis of different parts of the intact algal crust. This enables detection of small amounts of locally concentrated mineral that may not be above detection level (~1%) in standard powder XRD. Micro-XRD analyses were carried out using a
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FIG. 1. Polystrata dura encrusting coral. (A) Encrusting P. dura (Po) overgrowing coral branch with thin layer of Mg-calcite CCA between coral and P. dura, scale = 1 cm. (B) Backscatter SEM of P. dura crust showing growth layers (arrows), and (dark gray) magnesium-rich cells, scale = 200 lm. Backscatter SEM shows the lighter elements (i.e., magnesium) as darker gray, whereas heavier elements (i.e., calcium) are pale gray to white. (C) Secondary electron SEM image (showing topography of sample but providing no information on elemental composition) of uppermost layer of P. dura crust in radial vertical section showing monostromatic ventral perithallus (vp) below larger celled mesothallus (m), scale = 20 lm. Secondary electron images. (D) Backscatter SEM of cells 100 lm below crust surface. Magnesium-rich brucite (b) intracellular infill appears black, and aragonite (a) light gray, scale = 10 lm. (E) Intracellular cell infill (c) by magnesium minerals, scale = 2 lm.
Rigaku Rapid II XRD system with a 2-D image plate (Mo K radiation) at the Department of Geoscience, and Materials Science Program, University of Wisconsin. Powder XRD of the P. dura crust revealed the presence of aragonite (78% by weight of total sample) and Mg-calcite (22% weight). Very slight asymmetry on the lower 2-theta side of the Mgcalcite peak indicated the presence of calcite; however, this was not quantified separately. SEMEDS showed the P. dura crust was
aragonite (Fig. 1D), while the Mgcalcite was from crustose coralline algae (CCA) crust growth between the P. dura crust and the coral substrate (Fig. 1A). An additional material was detected within the cells of the P. dura crust. This substance was fluffy in appearance and magnesium rich (>95 mol% Mg 3–5 mm) of encrusting coralline algae were not present. A subsequent survey the following year also did not return thick crusts; unfortunately, the analysis presented here was not completed until after the second trip, so the significant presence of P. dura was not understood prior to the sec-
ond trip, and as such, there was no specific effort to look for thicker crusts. It is possible that CCA are forming thick crusts in the region but may not be abundant. However, this apparent absence of thick CCA crusts could indicate marine or ecosystem conditions in this particular location that inhibit Mg-calcite calcification or the sufficient preservation of their crusts to enable a build-up of carbonate (i.e., thick crusts). For example, Pueschel and Saunders (2009) speculated that the Ramicrusta textilis (a crustose peyssonnelioid) overgrowing corals in Jamaica may have been a recent shift as part of a conversion of coral-dominated reefs to algal dominated reefs. Pueschel and Saunders (2009) also observed a species of Polystrata overgrowing CCA. In the present study, the other peyssonnelioid samples from the control site analyzed by bulk XRD (n = 8) had Mg-calcite quantities ranging from 2 to 14 weight % of the total sample, indicating that CCA and peyssonnelioid mixed crusts are common in this area. However, three of the four peyssonnelioid samples from the CO2 vent site contained no Mg-calcite, suggesting the mixed crusts are potentially less common at the high CO2 sites. Unlike Jamaican reefs, there is no detailed historical information on the ecology of reefs in Papua New Guinea, and therefore, it is not known whether this mixed growth is typical or a recent shift. It may also be that absence of thick crusts by Mg-C CCA is typical for this area for reasons presently unknown. As the Mg-C CCA thick crusts were absent from both control and the CO2 vent sites, the absence is probably not directly related to carbonate saturation state. The mechanism driving brucite precipitation has not been identified but could be related to the presence of organic molecules that have been shown to induce nucleation of Mg-rich minerals (Tesson et al. 2008, Nash et al. 2011, Zhang et al. 2012). There was no visual evidence that the
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We thank K. E. Fabricius and the Australian Institute of Marine Sciences for providing us with the opportunity to visit the sites in Papua New Guinea. We would also like to thank Gary Saunders and the Connell Memorial Herbarium for storing the voucher. BDR was funded by an ARC Discovery Project and KRD by an ABRS National Taxonomy grant. SEM and XRD analysis was supported by the Electronic Materials Engineering Department, Research School of Physics and Engineering, ANU.
MERINDA C. NASH Research School of Physics and Engineering, Australian National University, Canberra, Australian Capital Territory, 0200, Australia BAYDEN D. RUSSELL The Environment Institute and School of Biological Sciences, The
University of Adelaide, Adelaide, South Australia, 5005, Australia Swire Institute of Marine Science and School of Biological Sciences, The University of Hong Kong, Hong Kong, China KYATT R. DIXON University of New Brunswick, Fredericton, NB, Canada E3B 5A3 MINGLULIU AND HUIFANG XU Department of Geoscience and Materials Science Program, University of Wisconsin, Madison 1215 West Dayton Street, Madison, Wisconsin, 53706-1600, USA Received 2 October 2014. Accepted 24 February 2015. Editorial Responsibility: M. Graham (Co-Editor) Al-Kawaz, H. A. 2010. Dissolution rate constant of carbonates under natural environments. Tikrit J. Pure Sci. 15:84– 90. Basso, D. 2012. Carbonate production by calcareous red algae and global change. Geodiversitas 34:13–33. Bilan, M. I. & Usov, A. I. 2001. Polysaccharides of calcareous algae and their effect on the calcification process. Russ. J. Bioorganic Chem. 27:2–16. Fabricius, K. E., Langdon, C., Uthicke, S., Humphrey, C., Noonan, S., De’ath, G., Okazaki, R., Muehllehner, N., Glas, M. S. & Lough, J. M. 2011. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nat. Clim. Change 1:165–9. Denizot, M. 1968. Les algues floridees encroutantes (a l’exclusion des Corallinacees). Museum national d’ Histoire naturelle, Paris, 310 pp. Heydrich, F. 1905. Polystrata, eine Squamariacee aus den tropen. Berichte der deutsche botanischen Gesellschaft 23:30–6. James, N. P., Wray, J. L. & Ginsburg, R. N. 1988. Calcification of encrusting aragonitic algae (Peyssonneliaceae): implications for the origin of Late Paleozoic reefs and cements. J. Sed. Pet. 58:291–303. Kato, A., Baba, M., Kawai, H. & Masuda, M. 2006. Reassessment of the littleknown crustose red algal genus Polystrata (Gigartinales), based on morphology and SSU rDNA sequences. J. Phycol. 42:922–33.
Krayesky, D. M., Norris, J. N., Gabrielson, P. W., Gabriel, D. & Fredericq, S. 2009. A new order of red algae based on the Peyssonneliaceae, with an evaluation of the ordinal classification of the Florideophyceae (Rhodophyta). Proc. Biol. Soc. Washington 122:364–91. Morse, J. W., Arvidson, R. S. & Luttge, A. 2007. Calcium carbonate formation and dissolution. Chem. Rev. 107:342–81. Nash, M. C., Opdyke, B. N., Troitzsch, U., Russell, B. D., Adey, W. H., Kato, A. & Kline, D. I. 2013b. Dolomite-rich coralline algae in reefs resist dissolution in acidified conditions. Nat. Clim. Change 3:268–72. Nash, M. C., Opdyke, B. N., Wu, Z., Xu, H. & Trafford, J. M. 2013a. Simple X-ray diffraction techniques to identify mgcalcite, dolomite, and magnesite in tropical coralline algae and assess peak asymmetry. J. Sed. Res. 83:1084–98. Nash, M. C., Troitzsch, U., Opdyke, B. N., Trafford, J. M., Russell, B. D. & Kline, D. I. 2011. First discovery of dolomite and magnesite in living coralline algae and its geobiological implications. Biogeosciences 8:3331–40. Nothdruft, L. & Webb, G. 2009. Earliest diagenesis in scleractinian coral skeletons: implications for palaeoclimate sensitive geochemical archives. Facies 55:161–201. Pueschel, C. M. & Saunders, G. W. 2009. Ramicrusta textilis sp. nov. (Peyssonneliaceae, Rhodophyta), an anatomically complex Caribbean alga that overgrows corals. J. Phycol. 48:480–91. Schmalz, R. F. 1965. Brucite in carbonate secreted by the red algae Goniolithon sp. Science 149:993–6. Stumm, W. & Morgan, J. J. 1995. Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters, 3rd edn. Wiley-Interscience, New York, New York. Tesson, B., Gaillard, C. & Martin-Jezequel, V. 2008. Brucite formation mediated by the diatom Phaeodactylum tricornutum. Mar. Chem. 109:60–76. Watt, W. M., Morrell, C. K., Smith, D. L. & Steer, M. W. 1987. Cystolith development and structure in Pilea cadierei (Urticaceae). Ann. Bot-London 60:71–84. Womersley, H. B. S. 1994. The Marine Benthic Flora of Southern Australia - Part IIIA - Bangiophyceae and Florideophyceae (Acrochaetiales, Nemaliales, Gelidiales, Hildenbrandiales and Gigartinales sensu lato). Australian Biological Resources Study, Canberra, 508 pp. Zhang, F., Xu, H., Konishi, H., Shelobolina, E. S. & Roden, E. E. 2012. Polysaccharide-catalyzed nucleation and growth of disordered dolomite: a potential precursor of sedimentary dolomite. Am. Mineral. 97:556–67.
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brucite infill is a result of alteration of the surrounding aragonite thallus. As this is the first record of brucite in Polystrata, or any member of the Peyssonneliales, it is not known whether the presence of brucite is unique to the algae in this region or present in Polystrata spp. from other localities. Because peyssonnelioid algae are presumed to be aragonitic, XRD is not a routine part of analysis, and thus, the brucite could well be abundant elsewhere. To further understand the occurrence of brucite, targeted survey work would be required to sample P. dura crusts around the PNG site and ideally comparative surveys in other tropical localities where thicker crust peyssonnelioid have been documented (e.g., Pueschel and Saunders 2009). It would also be interesting to compare dissolution rates of P. dura crusts with cell infill, to P. dura or other peyssonnelioids without cell infill, to test whether brucite infill is associated with increased resistance to dissolution.
