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Background Understanding the specificity and flexibility of the algal symbiosis-host association is fundamental for predicting how species occupy a diverse range of habitats. Here we assessed the algal symbiosis diversity of three species of larger benthic foraminifera from the genus Amphistegina and investigated the role of habitat and species identity in shaping the associated algal community. Results We used next-generation sequencing to identify the associated algal community, and DNA barcoding to identify the diatom endosymbionts associated with species of A. lobifera, A. lessonii, and A. radiata, collected from shallow habitats (A. lobifera and A. lessonii, while A. radiata specimens host predominately diatoms of the order Triceratiales. Conclusions We show that local habitat is the main factor influencing the overall composition of the algal symbiont community. However, host identity and the phylogenetic relationship among hosts is relevant in shaping the specific endosymbiont diatom community, suggesting that the relationship between diatom endosymbiont and hosts plays a crucial role in the evolutionary history of the genus Amphistegina. The capacity of Amphistegina species to associate with a diverse array of diatoms, and possibly other algal groups, likely underpins the ecological success of these crucial calcifying organisms across their extensive geographic range.

Large benthic foraminifera are major carbonate components in tropical carbonate platforms, important carbonate producers, stratigraphic tools and powerful bioindicators (proxies) of environmental change. The application of large benthic foraminifera in tropical coral reef environments has gained considerable momentum in recent years. These modern ecological assessments are often carried out by micropalaeontologists or ecologists with expertise in the identification of foraminifera. However, large benthic foraminifera have been under‐represented in favour of macro reef‐builders, for example, corals and calcareous algae. Large benthic foraminifera contribute about 5% to modern reef‐scale carbonate sediment production. Their substantial size and abundance are reflected by their symbiotic association with the living algae inside their tests. When the foraminiferal holobiont (the combination between the large benthic foraminifera host and the microalgal photosymbiont) dies, the remaining calcareous test renourishes sediment supply, which maintains and stabilizes shorelines and low‐lying islands. Geological records reveal episodes (i.e. late Palaeocene and early Eocene epochs) of prolific carbonate production in warmer oceans than today, and in the absence of corals. This begs for deeper consideration of how large benthic foraminifera will respond under future climatic scenarios of higher atmospheric carbon dioxide (pCO2) and to warmer oceans. In addition, studies highlighting the complex evolutionary associations between large benthic foraminifera hosts and their algal photosymbionts, as well as to associated habitats, suggest the potential for increased tolerance to a wide range of conditions. However, the full range of environments where large benthic foraminifera currently dwell is not well‐understood in terms of present and future carbonate production, and impact of stressors. The evidence for acclimatization, at least by a few species of well‐studied large benthic foraminifera, under intensifying climate change and within degrading reef ecosystems, is a prelude to future host–symbiont resilience under different climatic regimes and habitats than today. This review also highlights knowledge gaps in current understanding of large benthic foraminifera as prolific calcium carbonate producers across shallow carbonate shelf and slope environments under changing ocean conditions., Minerva Foundation http://dx.doi.org/10.13039/501100001658, Deutsche Forschungsgemeinschaft http://dx.doi.org/10.13039/501100001659

Larger benthic foraminifera (LBF) are important carbonate producers in tropical and subtropical settings and play a large role in the carbon cycle. They suffer from bleaching (the expulsion/loss of the photosymbiotic microalgae) under increased sea surface temperature due to climate change. For artificial bleaching experiments, we used the diatom-bearing foraminiferan Amphistegina lobifera, because of its robustness in the laboratory for symbiosis investigations, and also the more sensitive Sorites orbiculus which hosts endosymbiotic dinoflagellates. In order to induce bleaching, the LBF were exposed to menthol at non-lethal concentrations. Additionally, DCMU (3-(3,4-dichlorophenyl)-1,1-dimethylurea) was applied as a photosynthetic inhibitor. After the 6 week experiment, foraminifera were >95% bleached, visible with the flourescence microscope. Survival rate of protists was high, as pseudopodial movement was still visible. The foraminifer in this bleached state was able to move and extend its pseudopodial network. The next step will be to test symbiont-uptake of those bleached foraminifera, and measure survival time and ecophysiological features of re-infected foraminifera.

Understanding the role of dispersal and adaptation in the evolutionary history of marine species is essential for predicting their response to changing conditions. We analyzed patterns of genetic differentiation in the key tropical calcifying species of large benthic foraminifera Amphistegina lobifera to reveal the evolutionary processes responsible for its biogeographic distribution. We collected specimens from 16 sites encompassing the entire range of the species and analyzed hypervariable fragments of the 18S SSU rDNA marker. We identified six hierarchically organized genotypes with mutually exclusive distribution organized along a longitudinal gradient. The distribution is consistent with diversification occurring in the Indo‐West Pacific (IWP) followed by dispersal toward the periphery. This pattern can be explained by: (a) high dispersal capacity of the species, (b) habitat heterogeneity driving more recent differentiation in the IWP, and (c) ecological‐scale processes such as niche incumbency reinforcing patterns of genotype mutual exclusion. The dispersal potential of this species drives the ongoing range expansion into the Mediterranean Sea, indicating that A. lobifera is able to expand its distribution by tracking increases in temperature. The genetic structure reveals recent diversification and high rate of extinction in the evolutionary history of the clade suggesting a high turnover rate of the diversity at the cryptic level. This diversification dynamic combined with high dispersal potential, allowed the species to maintain a widespread distribution over periods of geological and climatic upheaval. These characteristics are likely to allow the species to modify its geographic range in response to ongoing global warming without requiring genetic differentiation., Genetic differentiation and distribution of populations can provide clues about processes shaping species evolutionary histories. We examined the genetic signature of globally distributed species of large benthic foraminifera in order to identify mechanisms acting at geological and ecological time scales. We found that while dispersal capacity allows populations to extend their range, geographic distribution was strongly shaped by biogeographic breaks and niche incumbency.

Early‐diagenetic cementation of tropical carbonates results from the combination of numerous physico‐chemical and biological processes. In the marine phreatic environment it represents an essential mechanism for the development and stabilization of carbonate platforms. However, diagenetic cements that developed early in the marine phreatic environment are likely to become obliterated during later stages of meteoric or burial diagenesis. When lithified sediment samples are studied, this complicates the recognition of processes involved in early cementation, and their geological implications. In this contribution, a petrographic microfacies analysis of Holocene Halimeda segments collected on a coral island in the Spermonde Archipelago, Indonesia, is presented. Through electron microscopical analyses of polished samples, this study shows that segments are characterized by intragranular cementation of fibrous aragonite, equant High‐Mg calcite (3.9 to 7.2 Mol% Mg), bladed Low‐Mg calcite (0.4 to 1.0 Mol% Mg) and mini‐micritic Low‐Mg calcite (3.2 to 3.3 Mol% Mg). The co‐existence and consecutive development of fibrous aragonite and equant High‐Mg calcite results initially from the flow of oversaturated seawater along the aragonite template of the Halimeda skeleton, followed by an adjustment of cement mineralogy towards High‐Mg calcite as a result of reduced permeability and fluid flow rates in the pores. Growth of bladed Low‐Mg calcite cements on top of etched substrates of equant High‐Mg calcite is explained by shifts in pore water pH and alkalinity through microbial sulphate reduction. Microbial activity appears to be the main trigger for the precipitation of mini‐micritic Low‐Mg calcite as well, based on the presumable detection of an extracellular polymeric matrix during an early stage of mini‐micrite Low‐Mg calcite cement precipitation. Radiocarbon analyses of five Halimeda segments furthermore indicate that virtually complete intragranular cementation in the marine phreatic environment with thermodynamically/kinetically controlled aragonite and High‐Mg calcite takes place in about 100 years. Collectively, this study shows that early‐diagenetic cements are highly diverse and provides new quantitative constraints on the rate of diagenetic cementation in tropical carbonate factories., Deutsche Forschungsgemeinschaft http://dx.doi.org/10.13039/501100001659, https://doi.pangaea.de/10.1594/PANGAEA.923980

Reef-dwelling calcifiers face numerous environmental stresses associated with anthropogenic carbon dioxide emissions, including ocean acidification and warming. Photosymbiont-bearing calcifiers, such as large benthic foraminifera, are particularly sensitive to climate change. To gain insight into their responses to near-future conditions, Amphistegina lobifera from the Gulf of Aqaba were cultured under three pCO2 conditions (492, 963, 3182 ppm) crossed with two temperature conditions (28 °C, 31 °C) for two months. Differential protein abundances in host and photosymbionts were investigated alongside physiological responses and microenvironmental pH gradients assessed via proton microsensors. Over 1000 proteins were identified, of which &gt, 15% varied significantly between treatments. Thermal stress predominantly reduced protein abundances, and holobiont growth. Elevated pCO2 caused only minor proteomic alterations and color changes. Notably, pH at the test surface decreased with increasing pCO2 under all light/dark and temperature combinations. However, the difference between [H+] at the test surface and [H+] in the seawater—a measure of the organism’s mitigation of the acidified conditions—increased with light and pCO2. Combined stressors resulted in reduced pore sizes and increased microenvironmental pH gradients, indicating acclimative mechanisms that support calcite test production and/or preservation under climate change. Substantial proteomic variations at moderate-pCO2 and 31 °C and putative decreases in test stability at high-pCO2 and 31 °C indicate cellular modifications and impacts on calcification, in contrast to the LBFs’ apparently stable overall physiological performance. Our experiment shows that the effects of climate change can be missed when stressors are assessed in isolation, and that physiological responses should be assessed across organismal levels to make more meaningful inferences about the fate of reef calcifiers.

Background Revealing the specificity and flexibility of the algal symbiont-host association is fundamental for understanding how species can occupy a diverse range of habitats. Here we assessed the global distribution of the algal symbiont diversity for three shallow-water species of large benthic foraminifera (LBF) of the genus Amphistegina . Specifically, weinvestigated the role of habitat and host identity on the diversity of algal biome. Results Here we used next-generation sequencing to identify the algal biome in the species A. lobifera , A. lessonii , and A. radiata , collected from shallow habitats in 16 sites, spanning from the Mediterranean Sea to French Polynesia. Results showed the consistent presence of Fragilariales as the main algal taxa associated with all species across sites analysed. However, we uncovered unprecedented diversity of algal phylotypes found in low abundance.We further found high variability in algal biomes both within and between species and sites, indicating a substantial level of flexibility in symbiont associations. The effect of site was significant in all species analysed, and showed that local habitat is the main factor influencing the identity of algal symbionts. Symbiotic associations are also not constrained by the species identity nor the phylogenetic relationship among closely related hosts, suggesting symbiont identity plays a limited role in the evolutionary history of the genus Amphistegina . Conclusions We found that species of Amphistegina form flexible symbiotic relationship with algal taxa, which are primarily shaped by their local habitat. These observations strongly suggest that the capacity of Amphistegina species to utilise a diverse array of available symbionts likely underpins the ecological success of these crucial calcifying organisms across their extensive geographic range.

Adaptation, acclimatization and symbiont diversity are known to regulate thermal tolerance in corals, but the role of these mechanisms remains poorly constrained in other photosymbioses, such as large benthic foraminifera (LBFs), which are known to bleach at temperatures that are likely to be exceeded in the near future. LBFs inhabit a broad range of shallow-water settings. Within species, differences in thermal tolerance have been found among populations from different habitats, but it is not clear whether such differences occur among LBFs inhabiting similar habitats, but differing in other aspects, such as symbiont type. To this end, we compared responses to thermal stress in specimens from a population of Amphistegina lessonii, an abundant Indo-Pacific species, to specimens of Amphistegina gibbosa, its Atlantic counterpart, from a similar environment but two different water depths (5 and 18 m). Test groups of each species were exposed in a common experiment to three thermal stress scenarios over a four-week period. Growth, respiration, mortality and motility were measured to characterize the holobiont response. Coloration, photosynthesis and chlorophyll a content were measured to determine the response of the endosymbiotic diatoms. The photosymbionts were characterized by genetic fingerprinting. Our results show that, although groups of A. gibbosa were collected from different habitats, their responses were similar, indicating only marginally higher tolerance to thermal peaks in specimens from the shallower site. In contrast, species-specific differences were stronger, with A. lessonii showing higher tolerance to episodic stress and less pronounced impacts of chronic stress on motility, growth and photosymbiont performance. These interspecies variations are consistent with the presence of different and more diverse symbiont assemblages in A. lessonii compared with A. gibbosa. This study demonstrates the importance of considering symbiont diversity in the assessment of intra- and interspecific variations in stress responses in LBFs.

Tropical coastal ecosystems provide a unique complex marine habitat with a high diversity of algal species, Viet Nam being a particular hotspot. These algae may host a variety of potential unknown or underestimated bioactive algal compounds. In parallel the worldwide rising interest in macroalgae-based products leads to increasing activities in seaweed natural harvest and mariculture within coastal waters. With this growing interest, the present work provides baseline data for a systematic and science-based macroalgal monitoring program in Nha Trang Bay, Viet Nam, to keep track of potentially interesting taxa and to identify driving environmental factors which may also naturally influence biodiversity and species abundance. The present study investigated macrophyte diversity and abundance by combining a qualitative and quantitative macroalgal survey approach with environmental sampling (e.g. physicochemical properties of water column, underwater light regime, and sediment characteristics). Surveys were performed in the dry season (May/June) 2019 in different water depths (3, 6 and 10 m) at seven sites within Nha Trang Bay. The study revealed a coastal patchwork of diverse habitats inhabited by complex macrophyte communities, including estuarine dense Sargassum forests and Turbinaria meadows, sheltered sandy seagrass (Halodule spp.) beds with upcoming Lyngbya blooms, low diverse Padina deserts and highly turbid aquaculture (lobster and fish farms) impacted sites with surprisingly high macroalgal diversity. During our study a total of 86 macrophyte species were encountered in the subtidal (>1 m water depth), whereas only 6 species (Padina australis, Sargassum mcclurei, Turbinaria ornata, Halimeda discoidea, Amphiroa fragilissima, Tricleocarpa cylindrical) were frequently found at every survey site. The observed high patchiness and presence of economically important (e.g. Sargassum spp., Gracilaria spp., Caulerpa spp., Gelidiella acerosa, Acanthophora spicifera) and potentially economically interesting (e.g. Padina australis, Turbinaria ornata, Stypopodium zonale, Chondria armata) taxa during the survey underlines the high potential of the present macrophytic bio-resource, which apparently is strongly structured and will be altered by the changing heterogenic environment.

The dawn of animals remains one of the most mysterious milestones in the evolution of life. The fossil lipids 24-isopropylcholestane and 26-methylstigmastane are considered diagnostic for demosponges—arguably the oldest group of living animals. The widespread occurrence and high relative abundance of these biomarkers in Ediacaran sediments from 635–541 million years (Myr) ago have been viewed as evidence for the rise of animals to ecological importance approximately 100 Myr before their rapid Cambrian radiation. Here we show that the biosynthesis of 24-isopropylcholestane and 26-methylstigmastane precursors is common among early-branching unicellular Rhizaria—heterotrophic protists that play an important role in trophic cycling and carbon export in the modern ocean. Negating these hydrocarbons as sponge biomarkers, our study places the oldest evidence for animals closer to the Cambrian Explosion. Cambrian silica hexactine spicules that are approximately 535 Myr old now represent the oldest diagnostic sponge remains, whereas approximately 558-Myr-old Dickinsonia and Kimberella (Ediacara biota) provide the most reliable evidence for the emergence of animals. The proliferation of predatory protists may have been responsible for much of the ecological changes during the late Neoproterozoic, including the rise of algae, the establishment of complex trophic relationships and the oxygenation of shallow-water habitats required for the subsequent ascent of macroscopic animals. Fossil lipid biomarkers previously thought to be diagnostic of sponges (and thus indicative of animal life) are found to be preserved in unicellular Rhizarian protists, questioning a pre-Cambrian origin of sponges.

Background The classification of samples on a molecular level has manifold applications, from patient classification regarding cancer treatment to phylogenetics for identifying evolutionary relationships between species. Modern methods employ the alignment of DNA or amino acid sequences, mostly not genome-wide but only on selected parts of the genome. Recently proteomics-based approaches have become popular. An established method for the identification of peptides and proteins is liquid chromatography-tandem mass spectrometry (LC-MS/MS). First, protein sequences from MS/MS spectra are identified by means of database searches, given samples with known genome-wide sequence information, then sequence based methods are applied. Alternatively, de novo peptide sequencing algorithms annotate MS/MS spectra and deduce peptide/protein information without a database. A newer approach independent of additional information is to directly compare unidentified tandem mass spectra. The challenge then is to compute the distance between pairwise MS/MS runs consisting of thousands of spectra. Methods We present DISMS2, a new algorithm to calculate proteome-wide distances directly from MS/MS data, extending the algorithm compareMS2, an approach that also uses a spectral comparison pipeline. Results Our new more flexible algorithm, DISMS2, allows for the choice of the spectrum distance measure and includes different spectra preprocessing and filtering steps that can be tailored to specific situations by parameter optimization. Conclusions DISMS2 performs well for samples from species with and without database annotation and thus has clear advantages over methods that are purely based on database search. Electronic supplementary material The online version of this article (doi:10.1186/s12859-017-1514-2) contains supplementary material, which is available to authorized users.