Extreme cellular adaptations and cell differentiation required by a cyanobacterium for carbonate excavation

Abstract

Some cyanobacteria, known as euendoliths, excavate and grow into calcium carbonates, with their activity leading to significant marine and terrestrial carbonate erosion and to deleterious effects on coral reef and bivalve ecology. Despite their environmental relevance, the mechanisms by which they can bore have remained elusive and paradoxical, in that, as oxygenic phototrophs, cyanobacteria tend to alkalinize their surroundings, which will encourage carbonate precipitation, not dissolution. Therefore, cyanobacteria must rely on unique adaptations to bore. Studies with the filamentous euendolith, Mastigocoleus testarum, indicated that excavation requires both cellular energy and transcellular calcium transport, mediated by P-type ATPases, but the cellular basis for this phenomenon remains obscure. We present evidence that excavation in M. testarum involves two unique cellular adaptations. Long-range calcium transport is based on active pumping at multiple cells along boring filaments, orchestrated by the preferential localization of calcium ATPases at one cell pole, in a ring pattern, facing the cross-walls, and by repeating this placement and polarity, a pattern that breaks at branching and apical cells. In addition, M. testarum differentiates specialized cells we call calcicytes, that which accumulate calcium at concentrations more than 500-fold those found in other cyanobacteria, concomitantly and drastically lowering photosynthetic pigments and enduring severe cytoplasmatic alkalinization. Calcicytes occur commonly, but not exclusively, in apical parts of the filaments distal to the excavation front. We suggest that calcicytes allow for fast calcium flow at low, nontoxic concentrations through undifferentiated cells by providing buffering storage for excess calcium before final excretion to the outside medium.

Combined Effects of Experimental Acidification and Eutrophication on Reef Sponge Bioerosion Rates

“…It is likely that chip removal processes utilize products from the dissolution to contract their tissue and move the chip up from the boring pit into an excurrent canal. Work on phototrophic cyanobacteria showed that microbial excavation was achieved by transcellular Ca 2+ transport (Garcia-Pichel, 2006;GarciaPichel et al, 2010;Guida and Garcia-Pichel, 2016). We tentatively suggest that the excess in Ca 2+ derived from the dissolution in CaCO − 3 may be used by sponges to contract a conductive pathway, similarly to how muscle cell contract when triggered by an increase in intracellular Ca 2+ (Sommerville and Hartshorne, 1986).…”

“…carbonate dissolution, photosynthesis must therefore supply a high fraction of the energetic costs of the bioerosion process which may include ATP usage for active Ca 2+ and/or active proton pumping (Guida and Garcia-Pichel, 2016). Higher rates during the day at low and ambient pCO 2 indicate that the benefit of acquired energy from photosynthetic activity FIGURE 6 | Net respiration rates (Resp net ) during the day (dark orange), dark respiration rates (dark Resp) during the night (light orange) and gross photosynthesis (P gross ) of the holobiont (sponge + symbionts) ± SEM for each pCO 2 and eutrophication scenario.…”

Evidence of high Ca uptake by cyanobacteria forming intracellular CaCO3 and impact on their growth

“…Among cyanobacteria, the differentiated cells called calcicytes, observed in the filamentous euendolithic cyanobacterium Mastigocoleus testarum, have been measured to contain 100 fmol of Ca per cell, which measured ~1 × 10 3 μm 3 (Guida & Garcia‐Pichel, ). This represents 20 mg of Ca per g of dry weight, a value similar to that estimated for cyanobacteria forming intracellular ACC (Table ).…”

Conserved bacterial genomes from two geographically distinct peritidal stromatolite formations shed light on potential functional guilds

“…Endolithic bacteria bore into carbonate substrate through dissolution facilitated by uptake, transport and eventual release of calcium ions at the distal end of multicellular cyanobacterial trichomes (Fig. 3) [50, 51]. Increased concentration of free calcium ions at the surface of the stromatolite may promote calcium carbonate precipitation [31].…”

“…Increased concentration of free calcium ions at the surface of the stromatolite may promote calcium carbonate precipitation [31]. Certain genes are upregulated during this boring activity, including key genes encoding calcium ATPases and calcium-binding proteins [51, 52]. We identified an incredible 1 182 gene copies encoding calcium-binding proteins and 315 calcium ATPases in the putative genomes of bacteria from Cape Recife and Schoenmakerskop stromatolites.…”