Self-preservation strategies during bacterial biomineralization with reference to hydrozincite and implications for fossilization of bacteria

Abstract

The induction of mineralization by microbes has been widely demonstrated but whether induced biomineralization leads to distinct morphologies indicative of microbial involvement remains an open question. For calcium carbonate, evidence suggests that microbial induction enhances sphere formation, but the mechanisms involved and the role of microbial surfaces are unknown. Here, we describe hydrozincite biominerals from Sardinia, Italy, which apparently start life as smooth globules on cyanobacterial filaments, and evolve to spheroidal aggregates consisting of nanoplates. Complementary laboratory experiments suggest that organic compounds are critical to produce this morphology, possibly by inducing aggregation of nanoscopic crystals or nucleation within organic globules produced by metabolizing cells. These observations suggest that production of extracellular polymeric substances by microbes may constitute an effective mechanism to enhance formation of porous spheroids that minimize cell entombment while also maintaining metabolite exchange. However, the high porosity arising from aggregation-based crystal growth probably facilitates rapid oxidation of entombed cells, reducing their potential to be fossilized.

Microbial contribution to early marine cementation

“…Likewise, biologically formed ACC has been documented on crescent‐shaped bacillus (Diaz et al ., 2017) and on the cell surfaces of phototrophs, for example, cyanobacteria and diatoms (Figs 8J and 12B) where ACC nanograins can act as cell shields from uncontrolled precipitation (Obst et al ., 2009). While some argue that extracellular calcification is a ‘post‐mortem’ event, new evidence suggests otherwise (Obst et al ., 2009; Jones & Peng, 2014; Shiraishi et al ., 2020) because some mineralized cyanobacteria cells can efficiently support nutrient/metabolite exchange across extracellular mineral precipitates of porous nature (Ngwenya et al ., 2014). Most recently, it has been discovered that some species of cyanobacteria can form intracellular ACC precipitates within intracellular microcompartments, challenging the notion that ACC formation is exclusively extracellular (Couradeau et al ., 2012; Moreira et al ., 2017; Blondeau et al ., 2018).…”

Forced Biomineralization: A Review

“…In turn, the mesocrystals aggregate to form globules and sheaths all around the extracellular organic matrices on the surface of these microorganisms. These globules merge into each other as they grow and appear to maintain a smooth texture, with the porous structure only appearing at later stages of growth [ 98 ].…”

Origin of the Moroccan Touissit-Bou Beker and Jbel Bou Dahar Supergene Non-Sulfide Biomineralization and Its Relevance to Microbiological Activity, Late Miocene Uplift and Climate Changes

“…In fact, the development of these laminated rhythmically banded macrostructures that are very similar to nanotextures observed in recent bacterial biofilms are interpreted as fossil microbial mats that resulted from in situ metabolic products of sulfate-reducing/oxidizing bacteria and archaea (e.g., [22][23][24]). Similarly, the aforementioned macro-and microstructures are comparable to those described in biologically controlled hydrozincite-bearing mineralization whose genesis has been linked to photosynthetic alkalinization of the cyanobacterial cell surface during the seasonal alternation between spring and summer [92][93][94]. More interestingly, the stromatolitic-to peloïdallike textured smithsonite, which consists of a layered succession of alternating mm-to cm-thick laminae of white and colorless hydrozincite and smithsonite-2 (Figure 11B,C), could reflect seasonal variations in temperature and fluctuations in pH.…”

“…Thermochronological data [42][43][44][94][95][96][97][98][99] along with structural constraints indicate the involvement of a major pulse of exhumation (i.e., D 3 of [42]) that occurred during the last~10 Ma, from middle/late Miocene to present, at an approximative shortening rate of 2.6 mm/year [44]. Additionally, geological correlations and comparison to similar supergene ore deposit types in the Mediterranean basin (e.g., [93]) and North Africa (e.g., [123]) indicate that the emplacement of the "red ore stage" could have occurred during the Pliocene-Pleistocene (8-7 Ma, [93]), coincident with an episode of sea-level rise in the study area at about 8 Ma [28,124].…”