Unravelling the enigmatic origin of calcitic nanofibres in soils and caves: purely physicochemical or biogenic processes?

Abstract

Abstract. Calcitic nanofibres are ubiquitous habits of secondary calcium carbonate (CaCO3) accumulations observed in calcareous vadose environments. Despite their widespread occurrence, the origin of these nanofeatures remains enigmatic. Three possible mechanisms fuel the debate: (i) purely physicochemical processes, (ii) mineralization of rod-shaped bacteria, and (iii) crystal precipitation on organic templates. Nanofibres can be either mineral (calcitic) or organic in nature. They are very often observed in association with Needle Fibre Calcite (NFC), another typical secondary CaCO3 habit in terrestrial environments. This association has contributed to some confusion between both habits, however they are truly two distinct calcitic features and their recurrent association is likely to be an important fact to help understanding the origin of nanofibres. In this manuscript the different hypotheses that currently exist to explain the origin of calcitic nanofibres are critically reviewed. In addition to this, a new hypothesis for the origin of nanofibres is proposed based on the fact that current knowledge attributes a fungal origin to NFC. As this feature and nanofibres are recurrently observed together, a possible fungal origin for nanofibres which are associated with NFC is investigated. Sequential enzymatic digestion of the fungal cell wall of selected fungal species demonstrates that the fungal cell wall can be a source of organic nanofibres. The obtained organic nanofibres show a striking morphological resemblance when compared to their natural counterparts, emphasizing a fungal origin for part of the organic nanofibres observed in association with NFC. It is further hypothesized that these organic nanofibres may act as templates for calcite nucleation in a biologically-influenced mineralization process, generating calcitic nanofibres. This highlights the possible involvement of Fungi in CaCO3 biomineralization processes, a role still poorly documented at present-day. Moreover, on a global scale, the organomineralization of organic nanofibres into calcitic nanofibres might have a great, however overlooked, impact on the biogeochemical cycles of both Ca and C.

Assessment of the Potential Role of Streptomyces in Cave Moonmilk Formation

“…Unlike typical mineral deposits, moonmilk is present as a soft and pasty precipitate on cave surfaces and within pools (Richter et al, 2008 ; Cacchio et al, 2014 ). The origin of moonmilk has been controversial for many years due to the complex mineralogy, the atypical crystalline morphology, and also the size of its crystals (Verrecchia and Verrecchia, 1994 ; Canaveras et al, 1999 , 2006 ; Bindschedler et al, 2010 , 2014 ). Notably, moonmilk deposits are characterized by several crystal habits including nano-fibers, and micro-meter sized needle-fiber crystals in a form of monocrystalline rods and polycrystalline chains (Canaveras et al, 1999 , 2006 ; Bindschedler et al, 2010 , 2014 ).…”

“…The origin of moonmilk has been controversial for many years due to the complex mineralogy, the atypical crystalline morphology, and also the size of its crystals (Verrecchia and Verrecchia, 1994 ; Canaveras et al, 1999 , 2006 ; Bindschedler et al, 2010 , 2014 ). Notably, moonmilk deposits are characterized by several crystal habits including nano-fibers, and micro-meter sized needle-fiber crystals in a form of monocrystalline rods and polycrystalline chains (Canaveras et al, 1999 , 2006 ; Bindschedler et al, 2010 , 2014 ). While initially postulated as a speleothem of abiotic origin (Harmon et al, 1983 ; Borsato et al, 2000 ), recent studies attributed the genesis of moonmilk to indigenous microbial population (Canaveras et al, 2006 ; Cailleau et al, 2009 ; Baskar et al, 2011 ; Braissant et al, 2012 ).…”

“…Moonmilk was reported to host wide spectrum of microbiota, including Archaea, Bacteria, and Fungi (Rooney et al, 2010 ; Portillo and Gonzalez, 2011 ; Engel et al, 2013 ; Reitschuler et al, 2014 , 2015 , 2016 ; Axenov-Gibanov et al, 2016 ; Maciejewska et al, 2016 ). Among this microbiome, fungi, and filamentous microorganisms, particularly members of Actinobacteria phylum were reported to be possibly involved in the moonmilk genesis (Canaveras et al, 2006 ; Bindschedler et al, 2010 , 2014 ). Bindschedler et al ( 2010 , 2014 ) suggested that the presence of nano-fibers within the crystalline structure of moonmilk was associated with biomineralized fungal hyphae.…”

“…Among this microbiome, fungi, and filamentous microorganisms, particularly members of Actinobacteria phylum were reported to be possibly involved in the moonmilk genesis (Canaveras et al, 2006 ; Bindschedler et al, 2010 , 2014 ). Bindschedler et al ( 2010 , 2014 ) suggested that the presence of nano-fibers within the crystalline structure of moonmilk was associated with biomineralized fungal hyphae. The authors suggest that organized networks of nano-fibers, often observed in moonmilk, could represent fibrous fungal cell wall polymers, such as chitin and β-(1 → 3)glucans (Bindschedler et al, 2010 ).…”

Formation of Biofilms on Rocks in Karst Caves

“…Консистенция спелеотемы «лунное молоко» зависит от интенсивности инфильтрации, элементного состава природных вод и активности микроорганизмов. Наряду с физикохимическими факторами на формирование вто-ричных минералов, существенное влияние могут оказывать микроорганизмы, которые растворяют материнские породы и служат биокаталитическими центрами аккумуляции и кристаллизации многих элементов Вопросы, связанные с происхождением и составом «лунного молока» остаются дискуссионными из-за сложного минералогического состава, атипичной морфологии и размеров кристаллов, входящих в его состав [5].…”