Hyella Caespitosa Research Articles

Microbial Endoliths on East Adriatic Limestone Coast: Morphological vs. Molecular Diversity

ABSTRACTFor the first time, a combined genotype-phenotype diversity analysis of endolithic microorganisms by pyrosequencing and microscopy was carried out across the intertidal and supratidal ranges of the Adriatic limestone coast. The coastal profiles represent ecotones between the sea and land, which express gradients of water supply, solar illumination, and salinity. The use of scanning electron microscopy imagery of resin casts showed that euendolith penetration remained shallow in the uppermost zones and was progressively deeper in the lower ranges where the water supply was more frequent. Microbial genotypes and phenotypes along the coastal profile showed large differences in dominance of taxa, but less in their diversity. The linkage between morphotypes observed along the profile and sequences was achieved by sequencing single cells/filaments, which were morphologically identified prior to their amplification. Molecular signatures of Hormathonema spp., Hyella caespitosa, Scytonema endolithicum, Solentia paulocellulare and Kyrtuthrix dalmatica were found on the profile and their specific placement was confirmed by morphological observations. Most sequences obtained were affiliated with Cyanobacteria (43%), Alphaproteobacteria (18%), and Gammaproteobacteria (7%). A total of 13 cyanobacterial morphospecies and 17 genotypes were found. Most cyanobacterial sequences belonged to the Pleurocapsales (33%), only 2% of the sequences belonged to the Nostocales and Oscillatoriales. The sequences corresponding to the cyanobacterial genus Hormathonema exhibited the highest abundances among all detected sequences, which is consistent with the microscopic observations in other parts of the world. The results of our investigation underline the importance of a combined approach in comparing the molecular data with microscopic observations in all phases of the study. Further RNA studies are needed to identify the actively growing parts of the endolithic community.

Supratidal Extremophiles--Cyanobacterial Diversity in the Rock Pools of the Croatian Adria.

Hardly any molecular studies have been done on euendoliths of marine coastal environments, especially along the supratidal ranges of carbonate coasts. In our study, we provide a comparative sequence analysis using 454 pyrosequencing of the 16S ribosomal RNA (rRNA) gene combined with extensive microscopy of the endolithic community from rock pools of the Croatian Adria. Molecular diversity indices and richness estimates showed high level of diversity, particularly in high-salinity samples. The most common cyanobacteria belong to the order Pleurocapsales, similar to observations on limestone coasts in other parts of the world. Using single-cell amplification sequences of Hormathonema spp., Hyella caespitosa, and Kyrtuthrix dalmatica was for the first time introduced to the public GenBank.Microscopic investigations did not show qualitative variances in diversity among sites with different salinity but clear differences in prevalent organisms from similar environments suggesting that most of them are adapted to inhabit extreme, marine endolithic habitats and that similar species inhabit geographically separated but ecologically similar environments. This is a remarkable concordance rather seldom seen in molecular community studies in support of the hypothesis that endolithic ecosystems are seeded from a global meta-community.The relative diversity of the community is greater than those described from harsh endolithic habitats of cold and hot deserts. The maximum likelihood phylogenetic tree consisting of 166 operational taxonomic units (OTUs) at 96 % sequence similarity revealed 11 distinct clusters. Three clusters contained only epilithic or endolithic taxa, and five clusters contained mixed epilithic and endolithic taxa. Organisms clustered according to their taxonomic affiliations and not to their preferences to salt concentrations.

Life-history trait of the Mediterranean keystone species Patella rustica: growth and microbial bioerosion

The age and shell growth patterns in populations of Patella rustica of the Adriatic Sea were determined by analyzing the inner growth lines visible in shell sections. Marginal increment analysis showed annual periodicity with annual growth line being deposited in May. The growth analysis of 120 individual shells showed that 90.8 % of collected individuals were less than 4 years of age and only two individuals (1.6 %) were older than 6 years. Population structure was described and the generalized von Bertalanffy growth parameters were calculated: asymptotic length (L∞) was 38.22 mm and the growth constant (K) was 0.30 year-1. Growth performance index value of P. rustica (Ø’) was 2.64 and is among the lowest ranges reported for limpet species. Patella rustica shells were degraded to different degrees by microbial bioerosion. Microboring organisms identified were pseudofilamentous and filamentous cyanobacteria Hormathonema paulocellulare, Hyella caespitosa, Mastigocoleus testarum and Leptolyngbya sp. The overall intensity of infestation was relatively low, but increased in severity with shell length. The damage was most often restricted to the oldest parts of the shell, i.e. apex of the shell, posing difficulties in determining the exact position of the first growth line. The present study is first to introduce the use of inner growth lines in Patella rustica shell sections as a reliable method for age determination and it provides the first insight into the growth patterns of this keystone species while taking the interference of microbial shell bioerosion in consideration.

Microendolithic structures from the Fort Payne Formation (lower Mississippian), Kentucky and Tennessee: Implications for the paleoenvironment of carbonate mud-mounds

Resin cast embedment and naturally occurring internal molds have revealed an assemblage of microendoliths from the Lower Mississippian Fort Payne Formation. Microendoliths produced by the heterotrophs Orthogonum lineare, Orthogonum giganteum, and Saccomorpha clava dominate this unit, as well as the phototroph-produced traces Ichnoreticulina elegans and Fascichnus dactylus, a chlorophyte (Ostreobium quekettii) and cyanobacterium (Hyella caespitosa), respectively. They were found within a variety of fossil substrates, including solitary corals, bryozoans, brachiopods, and gastropods, with a notable absence in all trilobites and echinoderms. The Fort Payne from the Lake Cumberland/Dale Hollow region of southern Kentucky–northern Tennessee contains a suite of fossiliferous green shale deposits with isolated locations of enigmatic carbonate mud-mounds. The latter, commonly referred to as ‘Waulsortian’ mounds in other geographical areas, have been the center of much speculation in the past few decades, and the paleoenvironmental parameters behind their formation remain controversial. Using the aforementioned microendoliths, a sense of the light availability within the Illinois Basin can be determined. The assemblage of ichnotaxa uncovered is representative of light conditions spanning from dysphotic to aphotic. Using previously constrained depth parameters that indicate a depth of no more than 100m, a dysphotic environment suggests that the water column was eutrophic, presumably due to high productivity within the Illinois Basin. This would seem to corroborate several other inferences about the Early Mississippian, including the growing number of suspension feeding echinoderms, the restructuring of phytoplanktonic communities and increased nutrient flux from a developing terrigenous floral weathering regime in the Early Mississippian.

Incidence of damaging endolith infestation of the edible mytilid bivalve Modiolus barbatus

Endolith microboring infestation in bearded horse mussel Modiolus barbatus collected from Mali Ston Bay, Croatia during 2010 was studied for incidence and distribution of damage in bivalve shells and in relation to shell length and condition index. Macroscopic changes in colour and thickness of the inner shell surface were investigated in order to determine endolith presence and host response. Results showed a significant percentage of over 93% of shells to be infested by endoliths. Analyses of shells grouped by the degree of infestation showed that the majority of specimens were moderately infested, most commonly within the central area of the shell. Microboring endoliths were dominated by cyanobacteria Plectonema (Leptolyngbya) terebrans, Mastigocoleus testarum, Hyella caespitosa and by the green algae Phaeophila sp. and Ostreobium quekettii. In addition, characteristic scars were carved into the host shell by the boring bivalve Rocellaria dubia in over 40% of sampled shells. SEM photographs revealed added shell layer deposition in infested specimens; in some cases, a prismatic layer is formed on the inner shell surface. This study shows that the incidence of infestation increases with shell length and that the degree of endolith infestation has adverse effects on the condition index.

Bathymetric zonation of modern microborers in dead coral substrates from New Caledonia—Implications for paleodepth reconstructions in Holocene corals

Microboring endoliths were studied in dead modern corals collected at various depths and in growth position on La Surprise atoll in New Caledonia. Eight taxa of microborers were regularly observed: three cyanobacteria ( Hyella caespitosa, Mastigocoleus testarum, and Plectonema terebrans), two chlorophytes ( Ostreobium quekettii and Phaeophila dendroides) and three fungal forms ( Dodgella priscus, and two unidentified fungi). The relative abundance of each taxon was determined in the modern corals throughout the studied sampling interval (from 0 down to 40 m water depth). This allowed us to propose for the first time a bathymetric model based on microendolith assemblages colonizing in situ hard-substrates of corals. In this model, the occurrence of the cyanobacteria Hyella and Mastigocoleus indicates a bathymetric range from 0 down to a water depth of 3 and 6 m respectively. The chlorophyta O. quekettii, associated with the cyanobacterium P. terebrans and fungi, is dominant from 10 to 40 m depth, which is the lower limit of our sampling. The distribution ranges of individual taxa observed in the dead coral substrates from New Caledonia are much narrower than those reported in the literature for other substrates. The bathymetric model based on distribution of microborers in modern corals was then applied to interpret the trace assemblages of microborers observed in Holocene corals collected by drilling on two reef sites of New Caledonia : La Surprise islet, in the vicinity of the sampling sites of the modern corals, and the barrier reef of Bayes, on the NE coast of Grande Terre. The paleodepth interpretations performed at various levels along the cores allow identification of several shallowing-upward sequences during the last 7000 years of reef growth in New Caledonia. Differences in the thickness of these sequences between La Surprise and Bayes sites were interpreted as differences in the space available for accommodation between the two sites, in turn related to the differential subsidence that affected New Caledonia during Holocene times. The use of the microendolith trace assemblages in paleodepth reconstructions of Holocene reefs from New Caledonia allowed detection of relative sea level variations finer than those deduced from changes in coralgal assemblages.

Euendolithic shell-boring cyanobacteria and chlorophytes from the saline lagoon Ahivadolimni on Milos Island, Greece

Samples of typical estuarine mollusc shells (Cerastoderma glauca, Abra ovata and Hydrobia acuta), differing in appearance, size and age, were collected from littoral habitats of a saline water lagoon (Ahivadolimni on Milos Island, Greece). Each shell sample was examined for the distribution, frequency and taxonomy of its shell-boring cyanobacteria and chlorophytes, and the associated attached (epizoic) diatoms. The euendolithic microflora was extracted using Pereny's solution and observed by light microscopy (LM). The results of microbial penetration (traces of euendoliths) were examined by scanning electron microscopy (SEM) after a hypochlorite treatment. The three-dimensional patterns of microbial penetration (boring patterns) were investigated under SEM by applying the resin-casting technique for modern euendoliths. Of the five euendolithic cyanobacteria found, one (Cyanosaccus atticus) was established from Greek marine biotopes, three (Hyella caespitosa var. arbuscula, H. inconstans and H. reptans) are second records and new for Europe, whereas one cyanobacterium (Leptolyngbya terebrans = Plectonema terebrans) and the three euendolithic chlorophytes found (Phaeophila dendroides, Ostreobium quekettii and Gomontia polyriza) show a cosmopolitan distribution. A survey of the diatoms found as epizoic on the mollusc shells (30 taxa) shows that most of them are typical representatives of marine to brackish water of coasts and estuarine areas. A systematic account of all euendoliths found in the mollusc shells is given. The morphological variability of the cyanobacterium Hyella inconstans, and of the chlorophytes Ostreobium quekettii and Gomontia polyriza is presented, with extended taxonomic comments for the latter species. The susceptibility of molluscs to infestation, as well as the morphological variability, world distribution and penetration patterns of the euendoliths within the host mollusc shells are also discussed.

Checklist of the benthic marine and brackish Galician algae (NW Spain)

We present an annotated checklist of the benthic marine and brackish algae of the Galician coasts (Spain) based on literature records and new collections. This checklist includes 618 species: 118 Cyanophyta, 296 Rhodophyta, 127 Ochrophyta, and 77 Chlorophyta. The number of specific, infraspecific taxa, and stages is 643: 121 Cyanophyta, 309 Rhodophyta, 135 Ochrophyta, and 79 Chlorophyta. Hyella caespitosa var. nitida, Calothrix fasciculata, Gracilariopsis longissima, Compsonema minutum, and Sphacelaria tribuloides are new records for Galicia, and there are also some new provincial records. We state the presence of each species for Lugo (Lu), A Coruna (Co), and Pontevedra (Po) provinces. The number of species found in Galicia is high, since 85% of the species recorded for the warm-temperate NE Atlantic Ocean grow in Galicia. Biogeographical comments comparing the Galician data with the neighboring areas of Britain and Ireland, Basque coast, Portugal, southern Iberian Peninsula, Canary Islands and Atlantic coast of Morocco are given. Finally, we present lists of cold-temperate, warm-temperate, Lusitanic Province endemics, and alien species growing in Galicia.

Bioerosion of the coralline alga Hydrolithon onkodes by microborers in the coral reefs of Moorea, French Polynesia

Calcareous skeletons of the coralline alga Hydrolithon onkodes are colonised by a variety of microboring organisms including euendolithic algae. The species composition of microboring organisms as well as the boring patterns and the boring activity differ between live and dead coralline crusts. The microborers inhabiting the live crusts form an obvious, macroscopically visible green layer in the basal part of the crust, which is in contact with the substratum underneath. Some species, primarily Plectonema terebrans (83 %) and Ostreobium quekettii (7 %) grow from the inside towards the crust’s surface and produce a dense network of branched filaments. Following the death of the coralline alga, the skeletons are colonised at the surface and bored inward by the cyanobacteria Hyella caespitosa, Mastigocoleus testarum, P. terebrans and various chlorophyta. The bioerosive activity was determined using Image Analysis. Carbonate removal was estimated at 0.12 g CaCO 3·cm –3 in the live crusts compared to 0.49 in dead crusts. Changes in endolith distribution and floristic composition between live and dead crusts, as well as subsequent changes in filament diameters of the microboring algal communities and penetration depth of endoliths, could explain the significantly higher rate of bioerosion in dead crust versus live crust. Endolith activity was found to vary between live and dead crusts; while microborers are direct agents of bioerosion in both live and dead crusts by removing carbonate from the skeletons (8 to 32 % of the substratum, in volume), they indirectly increased bioerosion rate in dead crusts since they are themselves exposed to grazing by fish, echinoderms and molluscs.

Incidence and distribution of phototrophic shell-degrading endoliths of the brown mussel Perna perna

The incidence, distribution and infestation sequences of four endolithic cyanobacteria in the shells of the brown mussel Perna perna (L.) were studied along the south coast of South Africa. The incidence of endolith-infested shells varied significantly among the 21 study sites (∼23 to 95%), with highest infestation rates occurring on promontories and headlands as compared to sites within bays. At a smaller scale, the incidence of infested shells also varied with tidal height, being high at the upper tidal levels of mussel distribution and low or absent on the lowshore. The observation that small-scale variability in infestation rates was positively related to water movement suggested that physical damage to the outer protective periostracum of mussels may have facilitated colonisation by endoliths. This hypothesis was supported by the fact that shells with artificially damaged periostraca became infested at a greater rate than did control shells. Once colonisation by the filamentous cyanobacteria Plectonema terebrans, Hyella caespitosa and Mastigocoleus testarum had taken place, endoliths spread throughout the shell, causing progressive shell deformation and damage. Only older shells that were infested by the late successional, cavity-forming Pleurocapsa sp., however, exhibited severe shell deformations, became brittle and eventually fractured near the structurally important site of adductor muscle attachment. Heterotrophic endoliths typically associated with shell degradation in previous studies were extremely rare and if present did not contribute to shell disintegration. Although it is generally perceived that endolithic algae and cyanobacteria are restricted to the surface layers of shells by light limitation within the substratum, it is clear from this study that the interaction of a combination of factors (i.e. erosion of the periostracum, successional sequence of colonists and mechanical properties of the shell) may result in phototrophic endoliths causing severe shell degradation and eventually mussel mortality.

Biodegradation of shells of the black pearl oyster, Pinctada margaritifera var. cumingii, by microborers and sponges of French Polynesia

The composition, distribution and infestation sequence of organisms that destroy the commercially valuable shells of the black oyster Pinctada margaritifera var. cumingii Jameson, 1901 were studied. Three ecologically different groups of boring (euendolithic) organisms were identified: (1) phototrophic boring microorganisms (cyanobacteria, Hyella caespitosa, Hyella sp., Mastigocoleus testarum, Plectonema terebrans, and green algae, Phaeophila dendroides, Ostreobium quekettii); (2) heterotrophic boring microorganisms (fungi, Ostracoblabe implexa); (3) filter-feeding boring organisms (sponges, Cliona margaritiferae, C. vastifica). The phototrophic endoliths dominate the external pristmatic region of the shell, whereas the valuable interior nacreous region is attacked mainly by heterotrophs. Boring patterns reflect in part the shape and behaviour of the organisms and in part the structural properties of the shell, and inflict different types of damage. Infestation starts with microbial borers, which prepare the conditions for later invasion by more damaging clionid sponges. The infestation begins always at the apex, the oldest part of the shells, from which the periostracum is often removed by natural attrition or by cleaning procedure. The rate of bioerosion in 1 yr-old hatchery shells is 36 times higher than in natural populations.

Bathymetric Zonation and Paleoecological Significance of Microborings in Puerto Rican Shelf and Slope Sediments

Sediments collected from 63 sites on the Puerto Rican shelf and slope at depths ranging from intertidal to 530 m were analyzed for associated microborings. Scanning electron microscope examination of three dimensional plastic casts of microboring networks form the primary basis for this study. In all, 27 microboring forms are distinguished on the basis of size and shape of boring casts, mode of branching, overall boring pattern and associated accessory structures. Although most of the microborings exhibit wide bathymetric ranges, many of the forms tend to occur more abundantly within restricted depth zones, suggesting a three-fold subdivision. The upper photic zone assemblage (intertidal to 20 m) is characterized by the endolithic blue-green algae Hyella gigas, Hyella caespitosa, Hyella tenuoir, Hormathonema sp., and an unidentified endolith likely of algal origin (form D). The lower photic zone assemblage (20 m - 85 m) is characterized by the green algae Ostreobium quekettii and Codiolum polyrhizum , the Conchocelis -stage of an endolithic red alga, and a problematic algal form (A). The aphotic zone is characterized by the absence of algal borings and the presence of fungal form Il and a tubular form of uncertain affinity. Microborings in the upper photic zone are typically oriented perpendicular to substrate surfaces; those of the lower photic and aphotic zones parallel substrate surfaces and penetrate only slightly into substrate interiors. Microborings as trace fossils appear to have high paleoecologic potential inasmuch as they are believed to be biologically specific and often are morphologically distinctive. Microborings have been reported in sediments ranging in age form Cambrian to Holocene with many ancient endoliths resembling extant forms. Differences in direction of penetration between photic and aphotic endolithic organisms may be sufficient criteria for differentiating paleophotic zones in ancient carbonate sequences. A Pleistocene example is presented from the Fort Thompson Formation of south Florida which indicates that impregnation techniques utilized in endolithic analysis of modern sediments may find application in studies of ancient microboring assemblages.

Hyellazone and chlorohyellazole, two novel carbazoles from the blue-green alga [formula omitted][formula omitted] born. et flah.

The structures of two carbazoles, hyellazole and 6-chlorohyellazole, from the blue-green alga Hyella caespitosa are reported. The structure of 6-chlorohyellazole was solved by X-ray crystallographic methods.