Impact of a low salinity year on the metabolism of a hypersaline coastal lagoon (Brazil)

Araruama Lagoon is a large, continuously hypersaline coastal lagoon (mean salinity 52 g l^-1). However, during certain years the evaporation-precipitation balance is modified and results in lower salinity conditions, e.g. 1989–1990 when the mean salinity measured 41 g l^-1. These atypical conditions are responsible for a different behavior of the system, normally characterized by the presence of extensive microbial algal mats, low pelagic primary production compared to benthic primary production, and low turbidity. However, during this study (1989–1990), the presence of microbial algal mats was restricted to the shallow eastern embayment of the lagoon representing c.a. 8% of the total area, the mean concentration of suspended matter was relatively high (21.2 mg l^-1) when compared with a typical year, and primary production measured was 447 mg C m^-2 d^-1, higher than benthic primary production during hypersaline years. These conditions therefore influence the trophic state of the system, during low salinity conditions, the lagoon was meso-eutrophic.     

Prokaryotic diversity in one of the largest hypersaline coastal lagoons in the world

Araruama Lagoon is an environment characterized by high salt concentrations. The low raining and high evaporation rates in this region favored the development of many salty ponds around the lagoon. In order to reveal the microbial composition of this system, we performed a 16S rRNA gene survey. Among archaea, most clones were related to uncultured environmental Euryarchaeota. In lagoon water, we found some clones related to Methanomicrobia and Methanothermococcus groups, while in the saline pond water members related to the genus Haloarcula were detected. Bacterial community was dominated by clones related to Gamma-proteobacteria, Actinobacteria, and Synechococcus in lagoon water, while Salinibacter ruber relatives dominated in saline pond. We also detected the presence of Alpha-proteobacteria, Pseudomonas-like bacteria and Verrucomicrobia. Only representatives of the genus Ralstonia were cosmopolitan, being observed in both systems. The detection of a substantial number of clones related to uncultured archaea and bacteria suggest that the hypersaline waters of Araruama harbor a pool of novel prokaryotic phylotypes, distinct from those observed in other similar systems. We also observed clones related to halophilic genera of cyanobacteria that are specific for each habitat studied. Additionally, two bacterioplankton molecular markers with ecological relevance were analyzed, one is linked to nitrogen fixation (nifH) and the other is linked to carbon fixation by bacterial photosynthesis, the protochlorophyllide genes, revealing a specific genetic distribution in this ecosystem. This is the first study of the biogeography and community structure of microbial assemblages in Brazilian tropical hypersaline environments. This work is directed towards a better understanding of the free-living prokaryotic diversity adapted to life in hypersaline waters.     

Evidence that Early Carboniferous ostracods colonised coastal flood plain brackish water environments

A study of the stable isotope composition (δ¹⁸O, δ¹³C) of biogenic (ostracod, mollusc) and authigenic carbonates in the Ballagan Formation, Lower Carboniferous of Scotland, coupled with evidence from sedimentology and associated fossil fauna and flora, supports the argument that this formation was deposited in a coastal flood plain setting, in brackish (0.5 < 30‰ NaCl) and hypersaline (> 40‰ NaCl) waters, but in the absence of persistent normal marine conditions. The oxygen isotope data from the Ballagan Formation divide into three clusters: a diagenetic field defined by low δ¹⁸O (< − 11‰ VPDB); an intermediary field (δ¹⁸O − 11‰ to − 9‰) composed of a mixture of known primary and secondary (diagenetic) carbonates; and samples within the range of − 9‰ to − 4‰ which, as far as we can ascertain, are largely unaltered. No samples give typical Early Carboniferous δ¹⁸O marine values. Average marine carbonates from Europe have δ¹⁸O between − 4‰ to − 3‰. The Ballagan Formation carbonates were probably deposited in evaporated freshwater and/or brackish water. This conclusion is supported by the presence of evaporites (gypsum, anhydrite, halite pseudomorphs) and common desiccation-cracked mudstone surfaces throughout the Ballagan Formation, suggesting conditions of fluctuating salinity in ephemeral bodies of water. The stable isotope data support the notion that the ostracod assemblages of the Ballagan Formation were colonising brackish water and hypersaline ecologies on a coastal flood plain during the Early Carboniferous, a stage of development that may have encouraged their colonisation of fully non-marine (limnetic) environments during the later Carboniferous. The ostracods include cytherellacean and kloedenellacean species known from marginal marine sites elsewhere, but probably tolerant of brackish water, podocopid species such as ‘Bythocypris’ aequalis that may have been adapted for brackish water settings on coastal flood plains (ephemeral lakes and lagoons), and paraparchitacean-dominated assemblages that may signal harsh (hypersaline or desiccating) environments.     

Life cycle and production of Hydrobia acuta Drap. (Gastropoda: Prosobranchia) in a hypersaline coastal lagoon

The life cycle and annual production of Hydrobia acuta was studied in a hypersaline lagoon (s = 39 in summer), forming a part of solar salt works. Quantitative random samples were taken at regular intervals over a period of 15 months using a corer, and snails collected were counted and measured. Weight and biomass was calculated from a length-weight relationship and from measurements of ash content. H. acuta was a strictly annual species in the study lagoon. Recruitment takes place over a brief period in May and June, after which the breeding population dies. Growth of the new generation was slow during summer, probably due to the unfavourably high salinity. A period of rapid growth took place in autumn coinciding with a drop in salinity caused by rainfall. In winter Hydrobia hibernated by burrowing deeply into the sediment. Growth recommenced in spring when the lagoon was reflooded, but by this time the number of survivors was low.The maximum density of snails was 6 000 m^–2 and maximum biomass 500 mg organic dry wt · m^–2. Annual cohort production was estimated as 786 mg organic dry wt · m^–2 · a^–1. These figures are low compared to other studies on hydrobiid snails, and for production in inland waters, but the value for annual P/B = 4.5 is typical for a univoltine species. The relevance of the results to foraging by wading birds (the main consumers), is discussed.     

Hypersaline lagoons as conservation habitats: macro-invertebrates at Muni Lagoon, Ghana

A survey on the aquatic ecology of Muni Lagoon was carried out during the period December 1993 to July 1994. Samples of zooplankton, aufwuchs and benthos were taken from a number of stations, representative of the different habitat types that occurred in the lagoon. The aquatic invertebrate fauna of the lagoon is listed and the temporal and spatial distribution of the fauna is described. The fauna is depauperate and biodiversity was related closely to the hydrology and salinity of the lagoon waters. During the early part of the study period, with dry weather conditions, there was very little macro-invertebrate life within the waters of the lagoon. The invertebrate fauna was confined to crabs, which occupied the fringing vegetation in the southernmost portions of the lagoon. With the onset of rains and the flooding of the lagoon, the sand bar separating the lagoon from the sea was opened turning the lagoon into a tidal system. This event brought a radical change to the fauna of the lagoon with very diverse marine zooplankton in some stations. Within weeks, worms and juvenile crabs were found several kilometres inland from the sea opening, an indication of the rapid re-colonisation of a previously hypersaline environment. The anthropogenic threats to the aquatic portion of this Ramsar site have been assessed and prioritised.     

Diversity and phylogeny of percolomonads based on newly discovered species from hypersaline and marine waters

Percolomonads are common freshwater, marine and hypersaline tetraflagellated organisms. Current phylogenetic analyses of eukaryotes comprise only two species of this underinvestigated family. Here, we studied the morphology, salinity tolerance and 18S rDNA gene-based phylogeny of seven percolomonad cultures. We describe three new genera and five novel species of Percolomonadida based on phylogenetic distances and morphological characteristics: Barbelia atlantica, B. abyssalis, Lula jakobsenorum, Nakurumonas serrata and Percolomonas doradorae.The new species show features typical for percolomonads, one long flagellum for skidding, three shorter flagella of equal length and a ventral feeding groove. The new species comprise organisms living in marine and athalassic hypersaline waters with salinity ranging from 10 to 150 PSU. Based on these novel taxa, the taxonomy and phylogeny of Percolatea was extended and further resolved.     

Reduced salinities compromise the thermal tolerance of hypersaline specialist diving beetles

Inland saline waters are globally threatened habitats that harbour unique assemblages of specialist invertebrates. In many Mediterranean regions, irrigation associated with intensive agriculture is lowering the salinity of these habitats, resulting in the loss of their specialist biota, although the mechanisms by which reductions in salinity lead to species loss are poorly understood. In the present study, the effects of reduced salinity on the temperature tolerance and thermal acclimatory abilities of two related species of hypersaline water beetles, Nebrioporus baeticus (Schaum) and Nebrioporus ceresyi (Aubé), are explored. Both upper (UTL) and lower thermal limits (LTL) are assessed, and both salinity and temperature are found to influence the thermal biology of Nebrioporus. Mean UTLs are greater in individuals of both species acclimated at high salinities, with salinity appearing to be more important than acclimation temperature in determining UTL. In both taxa, the lowest mean LTLs are recorded in individuals acclimated at the highest salinities and lowest temperatures; temperature‐dependent acclimation is only reported after exposure to relatively high salinities. The data show that salinity influences the thermal tolerance and acclimatory ability of these hypersaline beetles, and that lowered salinity compromises the ability of adult Nebrioporus to cope with both heat and cold. Such an effect may partly explain why specialist species are lost from hypersaline habitats subject to salinity reductions, and suggests that ongoing reduction in salinity may compromise the ability of such specialist taxa to cope with rapid climate change.     

Global distribution of free-living microbial species

Species of large animals and plants have geographically restricted distributions, but it is unclear if this also applies to free-living micro-organisms. We have attempted to clarify this, by investigating the ciliated protozoa living in a habitat that is separated from northern Europe by geographical barriers and great distance - the sediment of a Holocene volcanic crater-lake with brackish water, in Australia. Of the 85 ciliate species recorded, none was 'new', and all (apart from one species previously described only from tropical Africa) are known from northern Europe. All species appear to have reached the crater by passive dispersal from other freshwater and marine environments. The significance of this finding lies in the fact that ciliates are among the largest and most fragile of microbes. If ciliate species have global distributions, it is likely that the same is true for the many smaller, more abundant and more easily dispersed microbial species, including bacteria. There is some support for this in the literature, and most species smaller than ca 1 mm may have global distributions. Biodiversity at the microbial level is fundamentally different from that of macroscopic animals and plants, and it may be difficult to make realistic extrapolations from the attributes of microbial communities, to biodiversity in general.     

The biology and evolution of Antarctic saline lakes in relation to salinity and trophy

. Five brackish to hypersaline lakes (Highway, Ace, Pendent, Williams and Rookery) in the Vestfold Hills, eastern Antarctica were investigated during the austral summer of 1999/2000. The aims were to characterise the functional dynamics of the plankton and gain an understanding of how the different environments in the lakes have led to the evolution of different communities. The plankton was dominated by microorganisms and differed across the salinity spectrum in relation to trophy, age and the presence of meromixis. However, some elements of the plankton were common to all of the lakes, e.g. the mixtrophic ciliate, Mesodinium rubrum, which reached abundances of 2.7᎒⁵ l^-1 and spanned a salinity gradient of 4-63‰. Marine dinoflagellate species also occurred in all of the lakes, often at high abundances in Highway Lake, Pendent Lake and Lake Williams. During December (mid-summer), primary production showed an increase along the salinity gradient from Highway Lake to Lake Williams; however, it was low in hyper-nutrified Rookery Lake because of the turbidity of the waters. Bacterial production followed the same trend and was extremely high in Rookery Lake (327 µg l^-1 h^-1 in January). The lakes possessed a marine microbial plankton that has become very simplified through time, and now contains a small number of highly successful species, which were pre-adapted to surviving in extreme Antarctic lakes.     

Observations on the ultrastructure, mode of infectivity and host range of xenosomes

Xenosomes are infectious bacterial-like symbionts that reside in the cytoplasm of certain strains of the marine hymenostome ciliate, Parauronema acutum. Ultrastructural studies of xenosomes of one such strain, P. acutum, 110/3, reveal that the particles possess a cell envelope whose outer membrane resembles that of Gramnegative bacteria. Unlike typical Gram-negative bacteria, however, xenosomes possess a much reduced ‘murein’ layer. The DNA is not located in a ‘nucleosome’ or ‘nuclear body’ as it is in most bacteria, but may be found dispersed throughout the internal contents of the particle. Xenosomes are capable of infecting several strains of Parauronema spp. and at least one other ciliate of marine origin, Miamiensis avidus, Ma. They are also capable of inhibiting the growth of certain marine ciliate strains, particularly those of the genus Uronema. Infectivity may be related to the fact that the particles are motile. When released from the host protozoan, they may be seen spinning or darting rapidly, suggesting the presence of a motile apparatus. Phosphotungstic acid staining of the released particles show that they do, indeed, possess bacterial-like flagella. The average number of flagella per particle observed was two, although some particles were seen with as many as five. A flagellum may occur at almost any point on the surface of the particle and is characteristically wider near its point of insertion into the cell envelope than it is near its tip. During normal growth in axenic culture, xenosomes are actively released into the ambient medium. Particles, thus released, rapidly lose their capacity to infect susceptible hosts, and this capacity parallels their ability to remain motile.     

Substrate type determines metagenomic profiles from diverse chemical habitats

Environmental parameters drive phenotypic and genotypic frequency variations in microbial communities and thus control the extent and structure of microbial diversity. We tested the extent to which microbial community composition changes are controlled by shifting physiochemical properties within a hypersaline lagoon. We sequenced four sediment metagenomes from the Coorong, South Australia from samples which varied in salinity by 99 Practical Salinity Units (PSU), an order of magnitude in ammonia concentration and two orders of magnitude in microbial abundance. Despite the marked divergence in environmental parameters observed between samples, hierarchical clustering of taxonomic and metabolic profiles of these metagenomes showed striking similarity between the samples (>89%). Comparison of these profiles to those derived from a wide variety of publically available datasets demonstrated that the Coorong sediment metagenomes were similar to other sediment, soil, biofilm and microbial mat samples regardless of salinity (>85% similarity). Overall, clustering of solid substrate and water metagenomes into discrete similarity groups based on functional potential indicated that the dichotomy between water and solid matrices is a fundamental determinant of community microbial metabolism that is not masked by salinity, nutrient concentration or microbial abundance.     

Ciliates along Oxyclines of Permanently Stratified Marine Water Columns

Studies of microbial communities in areas of the world where permanent marine water column oxyclines exist suggest they are “hotspots” of microbial activity, and that these water features and the anoxic waters below them are inhabited by diverse protist taxa, including ciliates. These communities have minimal taxonomic overlap with those in overlying oxic water columns. Some ciliate taxa have been detected in multiple locations where these stable water column oxyclines exist; however, differences in such factors as hydrochemistry in the habitats that have been studied suggest local selection for distinct communities. We compare published data on ciliate communities from studies of deep marine water column oxyclines in Caricao Basin, Venezuela, and the Black Sea, with data from coastal, shallower oxycline waters in Framvaren and Mariager fjords, and from several deep‐sea hypersaline anoxic basins in the Eastern Mediterranean Sea. Putative symbioses between Bacteria, Archaea, and ciliates observed along these oxyclines suggests a strategy of cooperative metabolism for survival that includes chemosynthetic autotrophy and exchanges of metabolic intermediates or end products between hosts and their prokaryotic partners.     

A quick and cost-effective method for modelling water renewal in shallow coral reef lagoons

Water renewal exerts a preponderant role in eutrophication, yet few hydrodynamic indicators exist for performing quick and cost-effective assessments of ecosystem vulnerability. Using field data, we closed the water budget of a shallow coral reef lagoon recently exposed to high levels of nutrient loading that triggered green tides. Then, we tested the relevance of modelling flushing-time, a proxy of water renewal, from oceanic and atmospheric open access data. Water inflows in the lagoon were mainly driven by waves breaking on exposed reefs, but tide and wind also influenced water renewal during low-wave periods. Modelling flushing-time as a function of the wave features (significant wave height, direction, and period), tide, and wind direction provided the most convincing model, with greater contribution of wave height, and adequately reproduced observations for an independent dataset. Using this model to hindcast flushing-time over the period 2000–2019 highlighted that green tides that recently struck the area in January 2018 and June 2019 followed periods of slow water renewal, which therefore contributed to amplify the blooms. The analysis also demonstrated that renewal events even slower than those recorded in 2018–2019 are frequent in this lagoon, which highlights the high vulnerability of this UNESCO World Heritage Site to other pulses of nutrient loading. Since the methodology developed in this study can be easily applied to many other coastal barrier and fringing reefs, it offers a promising perspective for quick and cost-effective assessments of coral reef vulnerability to eutrophication and other ecosystem crises magnified by slow water renewal.

     

Distribution of picophytoplankton communities from brackish to hypersaline waters in a South Australian coastal lagoon

Background

Picophytoplankton (i.e. cyanobacteria and pico-eukaryotes) are abundant and ecologically critical components of the autotrophic communities in the pelagic realm. These micro-organisms colonized a variety of extreme environments including high salinity waters. However, the distribution of these organisms along strong salinity gradient has barely been investigated. The abundance and community structure of cyanobacteria and pico-eukaryotes were investigated along a natural continuous salinity gradient (1.8% to 15.5%) using flow cytometry.

Results

Highest picophytoplankton abundances were recorded under salinity conditions ranging between 8.0% and 11.0% (1.3 × 10⁶ to 1.4 × 10⁶ cells ml^-1). Two populations of picocyanobacteria (likely Synechococcus and Prochlorococcus) and 5 distinct populations of pico-eukaryotes were identified along the salinity gradient. The picophytoplankton cytometric-richness decreased with salinity and the most cytometrically diversified community (4 to 7 populations) was observed in the brackish-marine part of the lagoon (i.e. salinity below 3.5%). One population of pico-eukaryote dominated the community throughout the salinity gradient and was responsible for the bloom observed between 8.0% and 11.0%. Finally only this halotolerant population and Prochlorococcus-like picocyanobacteria were identified in hypersaline waters (i.e. above 14.0%). Salinity was identified as the main factor structuring the distribution of picophytoplankton along the lagoon. However, nutritive conditions, viral lysis and microzooplankton grazing are also suggested as potentially important players in controlling the abundance and diversity of picophytoplankton along the lagoon.

Conclusions

The complex patterns described here represent the first observation of picophytoplankton dynamics along a continuous gradient where salinity increases from 1.8% to 15.5%. This result provides new insight into the distribution of pico-autotrophic organisms along strong salinity gradients and allows for a better understanding of the overall pelagic functioning in saline systems which is critical for the management of these precious and climatically-stress ecosystems.     

Abundance, distribution, and activity of Fe(II)-oxidizing and Fe(III)-reducing microorganisms in hypersaline sediments of Lake Kasin, southern Russia

The extreme osmotic conditions prevailing in hypersaline environments result in decreasing metabolic diversity with increasing salinity. Various microbial metabolisms have been shown to occur even at high salinity, including photosynthesis as well as sulfate and nitrate reduction. However, information about anaerobic microbial iron metabolism in hypersaline environments is scarce. We studied the phylogenetic diversity, distribution, and metabolic activity of iron(II)-oxidizing and iron(III)-reducing Bacteria and Archaea in pH-neutral, iron-rich salt lake sediments (Lake Kasin, southern Russia; salinity, 348.6 g liter(-1)) using a combination of culture-dependent and -independent techniques. 16S rRNA gene clone libraries for Bacteria and Archaea revealed a microbial community composition typical for hypersaline sediments. Most-probable-number counts confirmed the presence of 4.26 × 10(2) to 8.32 × 10(3) iron(II)-oxidizing Bacteria and 4.16 × 10(2) to 2.13 × 10(3) iron(III)-reducing microorganisms per gram dry sediment. Microbial iron(III) reduction was detected in the presence of 5 M NaCl, extending the natural habitat boundaries for this important microbial process. Quantitative real-time PCR showed that 16S rRNA gene copy numbers of total Bacteria, total Archaea, and species dominating the iron(III)-reducing enrichment cultures (relatives of Halobaculum gomorrense, Desulfosporosinus lacus, and members of the Bacilli) were highest in an iron oxide-rich sediment layer. Combined with the presented geochemical and mineralogical data, our findings suggest the presence of an active microbial iron cycle at salt concentrations close to the solubility limit of NaCl.     

Ecosystem indicators: Foraminifera,Thecamoebians and Diatoms from the Ologe Lagoon,Nigeria

The Ologe Lagoon in southwestern Nigeria is a natural habitat located closely to both residential and industrial estates. The lagoon is heavily affected by effluents of agricultural and industrial runoff including organochlorine compounds and heavy metals (chloropesticides, DDT and polychlorinated biphenyls, cadmium, manganese, zinc, copper, lead, iron and nickel). Ologe Lagoon is situated in a semi-isolated position and its brackish waters traverse several creeks and lagoons before it reaches the Atlantic Ocean. The lagoon experiences minor tidal but noticeable salinity and pH variations during the rainy season. During the dry season, however, the waters have a comparatively long resident time where sediments act as sink and aggregate contaminants over time. Investigations on benthic foraminifera, thecamoebian and diatom species were carried out to document the current status, composition, spatial distribution, and response of microfaunal assemblages to environmental stressors within the lagoon. The benthic foraminifer assemblage is composed of four highly specialized agglutinated species of Ammotium salsum, Miliammina fusca, Ammobaculites dilatatus and Ammobaculites aff. A. exiguus. They are present at all sample sites with varying abundances. The high abundance of Ammotium salsum is considered an indication of environmental stress. Thecamoebian species of Difflugia oblonga, Difflugia proteiformis and Pontigulasia compressa were also recorded in varying proportions and generally represent less than one percent of the total foraminifera/thecamoebian assemblage. The presence of marine brackish water larger siliceous diatoms of Actinoptychus and Campylodiscus species indicates an interaction between the lagoon and the marine waters although on the minimal scale with regards to actual salinity ranges. The faunal assemblages recovered are characterized by low species richness and alpha diversity indices and are typical of shallow, marginal-marine hyposaline environments. Numerical abundances and spatial distribution patterns suggest taxon-specific habitat preferences and highlight their potential for environmental monitoring studies.     

Environmental metabarcoding reveals heterogeneous drivers of microbial eukaryote diversity in contrasting estuarine ecosystems

Assessing how natural environmental drivers affect biodiversity underpins our understanding of the relationships between complex biotic and ecological factors in natural ecosystems. Of all ecosystems, anthropogenically important estuaries represent a ‘melting pot'' of environmental stressors, typified by extreme salinity variations and associated biological complexity. Although existing models attempt to predict macroorganismal diversity over estuarine salinity gradients, attempts to model microbial biodiversity are limited for eukaryotes. Although diatoms commonly feature as bioindicator species, additional microbial eukaryotes represent a huge resource for assessing ecosystem health. Of these, meiofaunal communities may represent the optimal compromise between functional diversity that can be assessed using morphology and phenotype–environment interactions as compared with smaller life fractions. Here, using 454 Roche sequencing of the 18S nSSU barcode we investigate which of the local natural drivers are most strongly associated with microbial metazoan and sampled protist diversity across the full salinity gradient of the estuarine ecosystem. In order to investigate potential variation at the ecosystem scale, we compare two geographically proximate estuaries (Thames and Mersey, UK) with contrasting histories of anthropogenic stress. The data show that although community turnover is likely to be predictable, taxa are likely to respond to different environmental drivers and, in particular, hydrodynamics, salinity range and granulometry, according to varied life-history characteristics. At the ecosystem level, communities exhibited patterns of estuary-specific similarity within different salinity range habitats, highlighting the environmental sequencing biomonitoring potential of meiofauna, dispersal effects or both.     

Parasites of recruiting coral reef fish larvae in New Caledonia

Recruiting coral reef fish larvae from 38 species and 19 families from New Caledonia were examined for parasites. We found 13 parasite species (Platyhelminthes: Monogenea, Cestoda and Trematoda) but no acanthocephalan, crustacean or nematode parasites. Over 23% of individual fish were infected. Didymozoid metacercariae were the most abundant parasites. We conclude that most of the parasites are pelagic species that become ‘lost’ once the fish larvae have recruited to the reef. Larval coral reef fish probably contribute little to the dispersal of the parasites of the adult fish so that parasite dispersal is more difficult than that of the fish themselves.