Cryptic Niches Research Articles

Biogenetic peloidal micrites within coral skeletons cause geochemical anomalies in reef limestones, Zhongsha Atoll, South China Sea

High-magnesian calcite (HMC) peloidal micrite is a ubiquitous synsedimentary cement observed in abundance in the Holocene cryptic niches of coral intraskeletal pores and borings at Zhongsha Atoll in the South China Sea. In this study, we assessed the petrographic and geochemical effects of these intraclasts during early diagenesis. Peloidal micrites with an average diameter of 20–40 μm were composed of radially arranged rhombic micro-crystals of HMC (∼20 mol% MgCO3) and massive micritic nuclei. Some living bacterial/algal clumps in peloidal micrites are associated with bioluminescence and manifest an organic-rich micro-environments. Fragmented calcified cyanobacterial sheaths, which are components of the peloidal nuclei, further enhance biogenetic carbonate precipitation throughout peloidal micrite formation. The stable isotope characteristics of the peloidal microfabrics (average δ13C of 2.55 ± 0.15‰ and δ18O of −1.64 ± 0.25‰) suggest that photosynthesis and heterotrophic decomposition promoted peloidal micrite precipitation by increasing the carbonate saturation. Plentiful peloidal micrites within the intraskeletal pores also influenced the geochemical signatures of the bulk reef limestone. Owing to the presence of mixed HMC peloidal micrites, the δ13C and δ18O values of the bulk limestone (0.26 ± 1.04 and-3.82 ± 1.02‰, respectively) were elevated and fluctuated widely compared with pristine coral skeletons (−3.43 ± 0.48‰ and − 5.75 ± 0.278‰, respectively). Enriched Mn and depleted Sr contents led to an increase in the Mn/Sr diagenetic proxy. The co-occurrence of HMC peloidal micrites and elevated Mg/Ca, Mn/Sr, δ13C, and δ18O ratios indicate that the HMC peloidal micrites played an essential role in these geochemical variations. We, therefore, propose performing a comprehensive diagenetic evaluation before geochemical analyses of reef limestone. In such cases, selective micro-analysis of pristine areas in altered limestone would yield more robust reconstructions based on corals.

Advancing Key Gaps in the Knowledge of Plasmodium vivax Cryptic Infections Using Humanized Mouse Models and Organs-on-Chips.

Plasmodium vivax is the most widely distributed human malaria parasite representing 36.3% of disease burden in the South-East Asia region and the most predominant species in the region of the Americas. Recent estimates indicate that 3.3 billion of people are under risk of infection with circa 7 million clinical cases reported each year. This burden is certainly underestimated as the vast majority of chronic infections are asymptomatic. For centuries, it has been widely accepted that the only source of cryptic parasites is the liver dormant stages known as hypnozoites. However, recent evidence indicates that niches outside the liver, in particular in the spleen and the bone marrow, can represent a major source of cryptic chronic erythrocytic infections. The origin of such chronic infections is highly controversial as many key knowledge gaps remain unanswered. Yet, as parasites in these niches seem to be sheltered from immune response and antimalarial drugs, research on this area should be reinforced if elimination of malaria is to be achieved. Due to ethical and technical considerations, working with the liver, bone marrow and spleen from natural infections is very difficult. Recent advances in the development of humanized mouse models and organs-on-a-chip models, offer novel technological frontiers to study human diseases, vaccine validation and drug discovery. Here, we review current data of these frontier technologies in malaria, highlighting major challenges ahead to study P. vivax cryptic niches, which perpetuate transmission and burden.

Cryptic niche differentiation of novel sediment ecotypes of Ruegeria pomeroyi correlates with nitrate respiration.

Marine intertidal sediments fluctuate in redox conditions and nutrient availability, and they are also known as an important sink of nitrogen mainly through denitrification, yet how denitrifying bacteria adapt to this dynamic habitat remains largely untapped. Here, we investigated novel intertidal benthic ecotypes of the model pelagic marine bacterium Ruegeria pomeroyi DSS-3 with a population genomic approach. While differing by only 1.3% at the 16S rRNA gene level, members of the intertidal benthic ecotypes are complete denitrifiers whereas the pelagic ecotype representative (DSS-3) is a partial denitrifier lacking a nitrate reductase. The intertidal benthic ecotypes are further differentiated by using non-homologous nitrate reductases and a different set of genes that allow alleviating oxidative stress and acquiring organic substrates. In the presence of nitrate, the two ecotypes showed contrasting growth patterns under initial oxygen concentrations at 1 vol% versus 7 vol% and supplemented with different carbon sources abundant in intertidal sediments. Collectively, this combination of evidence indicates that there are cryptic niches in coastal intertidal sediments that support divergent evolution of denitrifying bacteria. This knowledge will in turn help understand how these benthic environments operate to effectively remove nitrogen.

Hypolithic communities shape soils and organic matter reservoirs in the ice-free landscapes of East Antarctica

The soils of East Antarctica have no rhizosphere with the bulk of organo-mineral interactions confined to the thin microbial and cryptogamic crusts that occur in open or cryptic niches and are collectively known as biological soil crust (BSC). Here we demonstrate that cryptic hypolithic varieties of BSC in the Larsemann Hills of East Antarctica contribute to the buildup of soil organic matter and produce several types of continuous organogenous horizons within the topsoil with documented clusters of at least 100 m2. Such hypolithic horizons accumulate 0.06–4.69% of organic carbon (TOC) with isotopic signatures (δ13Corg) within the range of −30.2 – −24.0‰, and contain from 0 to 0.38% total nitrogen (TN). The properties of hypolithic organic matter alternate between cyanobacteria- and moss-dominated horizons, which are linked to the meso- and microtopography patterns and moisture gradients. The major part of TOC that is stored in hypolithic horizons has modern or centenary 14C age, while the minor part is stabilized on a millennial timescale through shallow burial and association with minerals. Our findings suggest that hypolithic communities create a “gateway” for organic carbon to enter depauperate soils of the Larsemann Hills and contribute to the carbon reservoir of the topsoil at a landscape level.

APPLICATION OF RAMAN SPECTROSCOPY IN COMPARISON BETWEEN CRYPTIC MICROBIALITES OF RECENT MARINE CAVES AND TRIASSIC PATCH REEFS

ABSTRACTMicrobialites are common carbonate structures in cryptic niches of marine environments throughout geological time. In this research we compare the microbialites of small bioconstructions (biostalactites) of modern submarine caves of Sicily with those developed in small crypts of Carnian patch reefs of the Dolomite Mountains (Heiligkreuz Formation, Alpe di Specie) using Raman spectroscopy, a method that allows in situ determination of the organic content of microbial components. This methodology partly solves the uncertainty of geomicrobiological studies that use bulk measurements (i.e., biomarker analyses), which make it difficult to associate mineral precipitates with a specific microbial process. In the modern marine caves, the complex biotic relationships among skeletal organisms (mainly serpulids) and microbial communities produced biostalactites in which microbially induced biomineralization is the consequence of autotrophic and chemoheterotrophic bacterial activities. Sulfate-reducing bacteria, fed by metazoan organic matter, flourish in millimetric oxygen-depleted cavities of the skeletal framework, and induce autochthonous micrite deposition and early stabilization of the biostalactites. Similar processes have been interpreted to induce the deposition of the microbialites in the Upper Triassic patch reefs of the Dolomites. These small shallow water reefs, made up mainly of scleractinian corals, sponges and red algae, hold a skeletal framework rich in millimeter- to centimeter-size cavities, ideal cryptic niches for growth of microbial communities. Specific sulfate-reducing bacteria biomarkers are first identified using bulk measurements obtained by solvent extraction. The subsequent in situ characterization of organic compounds through micro-Raman spectroscopy indicates the same biogeochemical signatures of the microbialites within the cryptic cavities of the biostalactites of modern marine caves as those inside the skeletal framework of Carnian patch reefs. These data, showing the same processes in Triassic and modern cryptic microenvironments, is evidence that the microbially mediated precipitation in confined environments is a process independent of geological time that further investigation may be able to test.

Cryptic encrusting communities in a Middle Devonian mesophotic paleoenvironment of the Holy Cross Mountains, Poland

The Middle Devonian (Givetian) chaetetid sponges and alveolitid tabulate corals that inhabited mesophotic paleoenvironments of the southern shelf of Laurussia (Holy Cross Mountains, Poland) have been studied with respect to encrustation patterns. These epibiotic communities are characterized by modest diversity and high dominance, and show distinct polarization with respect to the exposed and cryptic sides of the host's skeletons. The most abundant davidsoniid brachiopods and microconchids show strong preferences toward the lower (cryptic) sides, while auloporid tabulate corals dominate on the exposed sides of the hosts. The remaining and much rarer epibionts, cornulitids and rugose corals, show no clear preferences. In some shallow-water Silurian paleoenvironments, auloporids are known to dominate the cryptic sides of the hosts. Thus, considering the auloporid tabulates as photosymbiotic corals, their absence or rarity in the Middle Devonian cryptic habitats might have resulted from insufficient irradiance levels in otherwise depleted light conditions. As a result, the available space and lack or lower competition for the area with faster-growing colonial auloporids, enabled solitary encrusters to colonize the cryptic niches. The scarce bioerosion traces and rather low diversity of epibionts in our case may indicate that these mesophotic reefs developed in a nutrient-poor, oligotrophic habitats. The davidsoniid-dominated, cryptic encrusting communities were widespread in some paleoenvironments during the Middle Devonian, being known from both Laurussia and South China craton. However, such mesophotic cryptic communities, characterized by distinct polarization in comparison to open-surface environments, contrast with other Givetian deep-water, aphotic cryptic communities reported so far, where such polarization is hardly visible.

Alteration of rocks by endolithic organisms is one of the pathways for the beginning of soils on Earth

Subaerial endolithic systems of the current extreme environments on Earth provide exclusive insight into emergence and development of soils in the Precambrian when due to various stresses on the surfaces of hard rocks the cryptic niches inside them were much more plausible habitats for organisms than epilithic ones. Using an actualistic approach we demonstrate that transformation of silicate rocks by endolithic organisms is one of the possible pathways for the beginning of soils on Earth. This process led to the formation of soil-like bodies on rocks in situ and contributed to the raise of complexity in subaerial geosystems. Endolithic systems of East Antarctica lack the noise from vascular plants and are among the best available natural models to explore organo-mineral interactions of a very old “phylogenetic age” (cyanobacteria-to-mineral, fungi-to-mineral, lichen-to-mineral). On the basis of our case study from East Antarctica we demonstrate that relatively simple endolithic systems of microbial and/or cryptogamic origin that exist and replicate on Earth over geological time scales employ the principles of organic matter stabilization strikingly similar to those known for modern full-scale soils of various climates.

Metagenomic analysis provides insights into functional capacity in a hyperarid desert soil niche community

In hyperarid ecosystems, macroscopic communities are often restricted to cryptic niches, such as hypoliths (microbial communities found beneath translucent rocks), which are widely distributed in hyperarid desert environments. While hypolithic communities are considered to play a major role in productivity, the functional guilds implicated in these processes remain unclear. Here, we describe the metagenomic sequencing, assembly and analysis of hypolithic microbial communities from the Namib Desert. Taxonomic analyses using Small Subunit phylogenetic markers showed that bacterial phylotypes (93%) dominated the communities, with relatively small proportions of archaea (0.43%) and fungi (5.6%). Refseq-viral database analysis showed the presence of double stranded DNA viruses (7.8% contigs), dominated by Caudovirales (59.2%). Analysis of functional genes and metabolic pathways revealed that cyanobacteria were primarily responsible for photosynthesis with the presence of multiple copies of genes for both photosystems I and II, with a smaller but significant fraction of proteobacterial anoxic photosystem II genes. Hypolithons demonstrated an extensive genetic capacity for the degradation of phosphonates and mineralization of organic sulphur. Surprisingly, we were unable to show the presence of genes representative of complete nitrogen cycles. Taken together, our analyses suggest an extensive capacity for carbon, phosphate and sulphate cycling but only limited nitrogen biogeochemistry.

Ecology and biogeochemistry of cyanobacteria in soils, permafrost, aquatic and cryptic polar habitats

Polar Regions (continental Antarctica and the Arctic) are characterized by a range of extreme environmental conditions, which impose severe pressures on biological life. Polar cold-active cyanobacteria are uniquely adapted to withstand the environmental conditions of the high latitudes. These adaptations include high ultra-violet radiation and desiccation tolerance, and mechanisms to protect cells from freeze–thaw damage. As the most widely distributed photoautotrophs in these regions, cyanobacteria are likely the dominant contributors of critically essential ecosystem services, particularly carbon and nitrogen turnover in terrestrial polar habitats. These habitats include soils, permafrost, cryptic niches (including biological soil crusts, hypoliths and endoliths), ice and snow, and a range of aquatic habitats. Here we review current literature on the ecology, and the functional role played by cyanobacteria in various Arctic and Antarctic environments. We focus on the ecological importance of cyanobacterial communities in Polar Regions and assess what is known regarding the toxins they produce. We also review the responses and adaptations of cyanobacteria to extreme environments.

Soluble proteins control growth of skeleton crystals in three coralline demosponges

Calcified demosponges (coralline sponges, sclero-sponges), the first metazoa producing a carbonate skeleton, used to be important reef building organisms in the past. The relatives of this group investigated here,Spirastrella (Acanthochaetetes) wellsi, Astrosclera willeyana andVaceletia cf.crypta, are restricted to cryptic niches of modern Pacific coral reefs and may be considered as “living fossils’. They are characterized by a basic biologically controlled metazoan biomineralization process. Each of the investigated taxa forms its calcareous basal skeleton in a highly specialized way. Moreover, each taxon secretes distinct Ca2+-binding macromolecules which were entrapped within the calcium carbonate crystals during skeleton formation. Therefore these Ca2+-binding macromolecules were also described as intracrystalline macromolecules. When isolated and separated by SDS polyacrylamide gel electrophoresis, the organic skeleton matrix of the three species revealed to be composed of a respective distinct array of EDTA-soluble proteins. A single protein of 41 kDa was detected inS. wellsi, two proteins of 38 and 120 kDa inA. willeyana, and four proteins of 18 kDa, 30 kDa, 33 kDa, and 37 kDa inVaceletia sp. When run on IEF gel, the Ca2+-binding proteins gave staining bands at pH values between 5.25 and 5.65. As proved by anin vitro mineralization assay, the extracted proteins effectively inhibit CaCO3 and SrCO3 precipitation, respectively, in a saturated solution. Biochemical properties and behavior of the extracted proteins strongly suggest that they are involved in crystal nucleation and skeleton carbonate formation within the calcified sponges studied here.

Nature and environmental significance of microbialites in Quaternary reefs: the Tahiti paradox

Drill cores from the bamer reef-edge of Tahiti exhibit 85-93-m-thick coralgal sequences recording at least 13,500 years of continuous reef growth in optimal environmental conditions. The cored reef sequences form an overall shallowingupward succession with assemblages of branching or massive colonies of Porires at the base overlain by a robust-branching community (Acropom gr. dmmi/robirstn) heavily encrusted by coralline algae, sessile vermetid gastropods and arborescent foraminifers, which grew at depths less than 6 m. Microbialites generally form the last stage of encrustation of coral colonies, or more commonly, of related encrusting organisms, thus appearing as a major structural component of the reef sequence where they may locally form 809 of the rock by volume. They developed in an open cavity system of the reef framework with freely circulating normal-marine water. Microbialites include laminated crusts and clotted micritic masses, commonly associated in compound crusts, probably feflecting differences in the composition of the involved biological communities and in biomineralization processes that controlled the accretion of the crusts. The isotopic composition of the microbialites (+2.05 to +3.92% I they underwent also indivitlual processes of biominrlali2ation. Besicles the overall decrease in lizht and enqy conditions rttlecting progressive burial by conil growth, the widespread development of microbialites within the reef framework may be related to increased alkalinity and niitrient availability in interstitial waters due to temstrial groundwwr seepage and puiodic runoffs. The tlevelopment of micrubialites in the cryptic niches of the reef framework ceased about 6000 years

Cenomanian/Turonian sponge microbialite deep-water hardground community (Liencres, Northern Spain)

A benthic community of sessile metazoans dominated by coralline sponges (e.g.Acanthochaetetes andVaceletia) is found within a Cenomanian-Turonian deep water hardground succession cropping out at the coastal area of the Bay of Biscay near Santander. The characteristic K-strategic community exhibits a very close taxonomic relationship with modern communities from the Pacific realm, which allows for a comparison with Recent environmental conditions. The sponge community was associated with automicrites, microbialites, and thin mineralized limonitic biofilms. This biofacies is typically found in cryptic niches of reefal buildups (“telescoping”). The iron-rich biofilms had a strong electrochemical corrosive ability which explains the distinct submarine dissolution patterns. The hardground conditions are controlled, in part, by strong contour current regimes linked with extremely oligotrophic water masses. This system was established during the drowning of a distal carbonate ramp during the early Middle Cenomanian (A.rhotomagenese zone). In the uppermost portion of the hardground (Late Cenomaian, upperR. cushmani zone) the coralline sponge community was replaced by thick limonitic stromatolites with numerous encrusting foraminifera (Miniacina-type) and by colonies of the problematic iron bacteriumFrutexites. This event is accompanied by an increase of terrigenous influx and detrital glauconite, indicating a fundamental change in food web, and terminates the sponge dominated basal hardground interval. Thehardground was buried by hemipelagic sediments during the Middle Turonian (upperR. kallesi zone).