Regional occupancy in unicellular eukaryotes: a reflection of niche breadth,habitat availability or size‐related dispersal capacity?

1. The distribution patterns of unicellular and multicellular organisms have recently been shown to differ profoundly, with the former probably being mostly cosmopolitan, whereas the latter are mostly restricted to certain regions. However, the within‐region distribution patterns of these two organism groups may be rather similar. 2. We predicted that the degree of regional occupancy in unicellular eukaryotes would be related to niche characteristics, dispersal ability and size, as has been found previously for multicellular organisms. The niche characteristics we considered were niche position, that measures marginality in species habitat distribution, and niche breadth, that measures amplitude in species habitat distribution. Niche characteristics were determined using Outlying Mean Index (OMI) analysis. 3. We found that the regional occupancy in our model group of unicellular eukaryotes, stream diatoms, was primarily a reflection of the niche position of a species or, more generally, habitat availability. Thus, non‐marginal species (i.e. species that occupied common habitat conditions across the region) tended to be more widely distributed than marginal species (i.e. species that were restricted to a limited range of rare habitat conditions). This finding was further supported by the general linear model, with niche position, niche breadth, maximum size and attachment mode as explanatory variables: niche position was by far the most important variable accounting for variability in regional occupancy, with significant amounts of additional variation related to niche breadth and maximum size of diatoms. 4. Thus, the degree of regional occupancy among unicellular eukaryotes may be primarily governed by habitat availability, supporting former findings for multicellular organisms.     

Which functional processes control the short-term effect of grazing on net primary production in grasslands?

For unicellular organisms, a lack of effects of local species richness on ecosystem function has been proposed due to their locally high species richness and their ubiquitous distribution. High dispersal ability and high individual numbers may enable unicellular taxa to occur everywhere. Using our own and published data sets on uni- and multicellular organisms, we conducted thorough statistical analyses to test whether (1) unicellular taxa show higher relative local species richness compared to multicellular taxa, (2) unicellular taxa show lower slopes of the species:area relationships and species:individuals relationships, and (3) the species composition of unicellular taxa is less influenced by geographic distance compared to multicellular taxa. We found higher local species richness compared to the global species pool for unicellular organisms than for metazoan taxa. The difference was significant if global species richness was conservatively estimated but not if extrapolated, and therefore higher richness estimates were used. Both microalgae and protozoans showed lower slopes between species richness and sample size (area or individuals) compared to macrozoobenthos, also indicating higher local species richness for unicellular taxa. The similarity of species composition of both benthic diatoms and ciliates decreased with increasing geographic distance. This indicated restricted dispersal ability of protists and the absence of ubiquity. However, a steeper slope between similarity and distance was found for polychaetes and corals, suggesting a stronger effect of distance on the dispersal of metazoans compared to unicellular taxa. In conclusion, we found partly different species richness patterns among uni- and multicellular eukaryotes, but no strict ubiquity of unicellular taxa. Therefore, the effect of local unicellular species richness on ecosystem function has to be reanalyzed. Macroecological patterns suggested for multicellular organisms may differ in unicellular communities.     

Assembly rules and community models for unicellular organisms: patterns in diatoms of boreal streams

1. Many studies have addressed either community models (e.g. Clementsian versus Gleasonian gradients) or assembly rules (e.g. nestedness, checkerboards) for higher plant and animal communities, but very few studies have examined different non‐random distribution patterns simultaneously with the same data set. Even fewer studies have addressed generalities in the distribution patterns of unicellular organisms, such as diatoms. 2. We studied non‐randomness in the spatial distribution and community composition of stream diatoms. Our data consisted of diatom surveys from 47 boreal headwater streams and small rivers in northern Finland. Our analytical approaches included ordinations, cluster analysis, null model analyses, and associated randomisation tests. 3. Stream diatom communities did not follow discrete Clementsian community types, where multiple species occur exclusively in a single community type. Rather, diatom species showed rather individualistic responses, leading to continuous Gleasonian variability in community composition. 4. Although continuous variability was the dominating pattern in the data, diatoms also showed significant nestedness and less overlap in species distribution than expected by chance. However, these patterns were probably only secondary signals from species’ individualistic responses to the environment. 5. Although unicellular organisms, such as diatoms, differ from multicellular organisms in several biological characteristics, they nevertheless appear to show largely similar non‐random distribution patterns previously found for higher plants and metazoans.     

Microbes modeling ontogeny

Model organisms are central to contemporary biology and studies of embryogenesis in particular. Biologists utilize only a small number of species to experimentally elucidate the phenomena and mechanisms of development. Critics have questioned whether these experimental models are good representatives of their targets because of the inherent biases involved in their selection (e.g., rapid development and short generation time). A standard response is that the manipulative molecular techniques available for experimental analysis mitigate, if not counterbalance, this concern. But the most powerful investigative techniques and molecular methods are applicable to single-celled organisms (‘microbes’). Why not use unicellular rather than multicellular model organisms, which are the standard for developmental biology? To claim that microbes are not good representatives takes us back to the original criticism leveled against model organisms. Using empirical case studies of microbes modeling ontogeny, we break out of this circle of reasoning by showing: (a) that the criterion of representation is more complex than earlier discussions have emphasized; and, (b) that different aspects of manipulability are comparable in importance to representation when deciding if a model organism is a good model. These aspects of manipulability harbor the prospect of enhancing representation. The result is a better understanding of how developmental biologists conceptualize research using experimental models and suggestions for underappreciated avenues of inquiry using microbes. More generally, it demonstrates how the practical aspects of experimental biology must be scrutinized in order to understand the associated scientific reasoning.     

Correlation of codon biases and potential secondary structures with mRNA translation efficiency in unicellular organisms

Gene expression is known to correlate with the degree of codon bias in many unicellular organisms. However, such a correlation is not observed in some organisms. It was demonstrated that inverted complementary repeats within coding DNA sequences (ORFs) should be considered for proper estimation of the translation efficiency because they can form secondary structures that obstruct ribosome movement. A program was developed for estimating the potential expression of ORFs in unicellular organisms on the basis of their genome sequences. The program computes the elongation efficiency index (EEI) and takes into account three key factors: codon bias, the average number of inverted complementary repeats, and the free energies of potential stem-loop structures formed by these repeats. The influence of these factors on translation was numerically estimated. Their optimal ratio was computed for each organism. EEIs of 384 unicellular organisms (351 bacteria, 28 archaea, and 5 eukaryotes) were computed using the annotated genomes available from GenBank. Five potential evolutionary strategies of translational optimization were determined in the organisms studied. A considerable difference in preferential translational strategies was observed between bacteria and archaea. Significant correlations between EEIs and gene expression levels were shown for two species (Saccharomyces cerevisiae and Helicobacter pylori), using the available microarray data. The method allows the numerical estimation of the translation efficiency of an ORF and optimization of the nucleotide composition of heterologous genes in specified unicellular organisms. The program is available at http://wwwmgs.bionet.nsc.ru/mgs/programs/eei-calculator.     

PCR analysis of the distribution of unicellular cyanobacterial diazotrophs in the Arabian Sea

An oligonucleotide primer, NITRO821R, targeting the 16S rRNA gene of unicellular cyanobacterial N2 fixers was developed based on newly derived sequences from Crocosphaera sp. strain WH 8501 and Cyanothece sp. strains WH 8902 and WH 8904 as well as several previously described sequences of Cyanothece sp. and sequences of intracellular cyanobacterial symbionts of the marine diatom Climacodium frauenfeldianum. This oligonucleotide is specific for the targeted organisms, which represent a well-defined phylogenetic lineage, and can detect as few as 50 cells in a standard PCR when it is used as a reverse primer together with the cyanobacterium- and plastid-specific forward primer CYA359F (U. Nubel, F. Garcia-Pichel, and G. Muyzer, Appl. Environ. Microbiol. 63:3327-3332, 1997). Use of this primer pair in the PCR allowed analysis of the distribution of marine unicellular cyanobacterial diazotrophs along a transect following the 67 degrees E meridian from Victoria, Seychelles, to Muscat, Oman (0.5 degrees S to 26 degrees N) in the Arabian Sea. These organisms were found to be preferentially located in warm (>29 degrees C) oligotrophic subsurface waters between 0 and 7 degrees N, but they were also found at a station north of Oman at 26 degrees N, 56 degrees 35'E, where similar water column conditions prevailed. Slightly cooler oligotrophic waters (<29 degrees C) did not contain these organisms or the numbers were considerably reduced, suggesting that temperature is a key factor in dictating the abundance of this unicellular cyanobacterial diazotroph lineage in marine environments.     

Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell

Background  

Eukaryotes are classified as either haplontic, diplontic, or haplo-diplontic, depending on which ploidy levels undergo mitotic cell division in the life cycle. Emiliania huxleyi is one of the most abundant phytoplankton species in the ocean, playing an important role in global carbon fluxes, and represents haptophytes, an enigmatic group of unicellular organisms that diverged early in eukaryotic evolution. This species is haplo-diplontic. Little is known about the haploid cells, but they have been hypothesized to allow persistence of the species between the yearly blooms of diploid cells. We sequenced over 38,000 expressed sequence tags from haploid and diploid E. huxleyi normalized cDNA libraries to identify genes involved in important processes specific to each life phase (2N calcification or 1N motility), and to better understand the haploid phase of this prominent haplo-diplontic organism.     

Overview on introduced aquatic species in European navigational and adjacent waters

More than 1,000 non-indigenous aquatic species have been recorded, in total, from coastal Europe, i.e. navigational inland waterways for ocean-going vessels and adjacent water bodies in close proximity. Regions considered in this overview range from European Arctic waters to the Mediterranean Sea and Irish waters to the Black Sea. The majority of introduced taxa have been first recorded since the 1950s. Approximately 600 taxa (ranging from unicellular algae to vertebrates) are established with self-sustaining populations. The dominating group of exotic species across all seas is zoobenthos organisms. Introduction vectors are predominantly shipping (ballast water and hull fouling) and species movements for aquaculture or stocking purposes.     

Does the natriuretic peptide system exist throughout the animal and plant kingdom?

Natriuretic peptides (NPs) and their receptors have been identified in vertebrate species ranging from elasmobranchs to mammals. Atrial, brain and ventricular NP (ANP, BNP and VNP) are endocrine hormones secreted from the heart, while C-type NP (CNP) is principally a paracrine factor in the brain and periphery. In elasmobranchs, only CNP is present in the heart and brain and it functions as a circulating hormone as well as a paracrine factor. Four types of NP receptors are cloned in vertebrates. NPR-A and NPR-B are guanylyl cyclase-coupled receptors, whereas NPR-C and NPR-D have only a short cytoplasmic domain. NPs are hormones important for volume regulation in mammals, while they act more specifically for Na(+) regulation in fishes. The presence of NP and its receptor has also been suggested in the most primitive vertebrate group, cyclostomes, and its molecular identification is in progress. The presence of ANP or its mRNA has been reported in the hearts and ganglia of various invertebrate species such as mollusks and arthropods using either antisera raised against mammalian ANP or rat ANP cDNA as probes. Immunoreactive ANP has also been detected in the unicellular Paramecium and in various species of plants including Metasequoia. Furthermore, the N-terminal prosegments of ANP, whose sequences are scarcely conserved even in vertebrates, have also been detected by the radioimmunoassay for human ANP prosegments in all invertebrate and plant species examined including Paramecium. Although these data are highly attractive, the current evidence is too circumstantial to be convincing that the immunoreactivity truly originates from ANP and its prosegments in such diverse organisms. The caution that has to be exercised in identification of vertebrate hormones from phylogenetically distant organisms is discussed.     

Geographical patterns of micro‐organismal community structure: are diatoms ubiquitously distributed across boreal streams?

A topic under intensive study in community ecology and biogeography is the degree to which microscopic, as well as macroscopic organisms, show spatially-structured variation in community characteristics. In general, unicellular microscopic organisms are regarded as ubiquitously distributed and, therefore, without a clear biogeographic signal. This view was summarized 75  years ago by Baas-Becking, who stated "everything is everywhere, but, the environment selects". Within the context of metacommunity theory, this hypothesis is congruent with the species sorting model. By using a broad-scale dataset on stream diatom communities and environmental predictor variables across most of Finland, our main aim was to test this hypothesis. Patterns of spatial autocorrelation were evaluated by Moran's I based correlograms, whereas partial regression analysis and partial redundancy analysis were used to quantify the relative importance of environmental and spatial factors on total species richness and on community composition, respectively. Significant patterns of spatial autocorrelation were found for all environmental variables, which also varied widely. Our main results were clear-cut. In general, pure spatial effects clearly overcame those of environmental effects, with the former explaining much more variation in species richness and community composition. Most likely, missing environmental variables cannot explain the higher predictive power of spatial variables, because we measured key factors that have previously been found to be the most important variables (e.g. pH, conductivity, colour, phosphorus, nitrogen) shaping the structure of diatom communities. Therefore, our results provided only limited support for the Baas-Becking hypothesis and the species sorting perspective of metacommunity theory.     

Scaling of energy metabolism in unicellular organisms: a re-analysis

The database used by Hemmingsen (1960) to compute energy metabolism in unicellular organisms was reassembled and submitted to linear (log-log) analysis. As Hemmingsen noted, this data set includes marine zygotes, which are not unicellular organisms. If no temperature correction factors are applied to the data the best-fit regression line has a slope of 0.698 +/- 0.024. Application of the temperature correction factors assumed to have been used by Hemmingsen gave a slope of 0.756 +/- 0.021, identical to the value he reported. The correlation coefficient is 0.97. The mean scatter about the regression line exceeds 100%. A revised set of temperature correction factors gave a slope of 0.730 +/- 0.021, suggesting that the value of almost exactly three-quarters obtained by Hemmingsen was probably fortuitous. The slope of the best-fit regression line is very sensitive to the inclusion of bacteria and flagellates. When the data points for these organisms are omitted from the calculation the slope decreases to 0.645 +/- 0.045. When the data points for bacteria, flagellates and marine zygotes are omitted, the slope drops to 0.608 +/- 0.025. The correlation coefficient (0.97), compared to the best-fit line reported by Hemmingsen, is unaffected; the mean deviation about the regression line drops to 40% and the points are evenly distributed about the regression line. Because of the small number of species for which measurements have been made, the existing database relating energy metabolism to cell size is not representative of unicellular organisms generally. It is concluded that the case for a three-quarters power rule expressing energy metabolism as a function of size in unicellular organisms generally is not at all persuasive.     

Who am I — and if so, how many? Species diversity of calcareous dinophytes (Thoracosphaeraceae, Peridiniales) in the Mediterranean Sea

The diversity of extant calcareous dinophytes (Thoracosphaeraceae, Dinophyceae) is not fully recorded at present. The establishment of algal strains collected at multiple localities is necessary for a rigorous study of taxonomy, morphology and evolution in these unicellular organisms. We collected sediment and water tow samples from more than 60 localities in coastal areas of the eastern Mediterranean Sea and documented 15 morphospecies of calcareous dinophytes. Internal transcribed spacer (ITS) barcoding identified numerous species of the Scrippsiella trochoidea species complex that were genetically distinct, but indistinguishable in gross morphology (i.e. with the same tabulation patterns of the motile theca and similar spiny coccoid stages). We assessed a possible minimal number of cryptic species using ITS ribotype networks that indicated the existence of at least 21 species within the Scrippsiella trochoidea species complex. Species diversity of calcareous dinophytes appears higher in the Mediterranean Sea than in other parts of the world??s oceans such as the North Sea. Our data underline the importance of field work to record the diversity of calcareous dinophytes and other unicellular life forms.     

DNA metabarcoding focused on difficult-to-culture protists: An effective approach to clarify biological interactions

DNA metabarcoding on a single organism is a promising approach to clarify the biological interactions (e.g., predator–prey relationships and symbiosis, including parasitism) of difficult-to-culture protists. To evaluate the effectiveness of this method, Radiolaria and Phaeodaria, which are ecologically important protistan groups, were chosen as target taxa. DNA metabarcoding on a single organism focused on the V9 region of the 18S rRNA gene revealed potential symbionts, parasites and food sources of Radiolaria and Phaeodaria. Previously reported hosts and symbionts (parasites) were detected, and newly recognized combinations were also identified. The contained organisms largely differed between Radiolaria and Phaeodaria. In Radiolaria, members of the same order tended to contain similar organisms, and the taxonomic composition of possible symbionts, parasites, and food sources was fixed at the species level. Members of the same phaeodarian family, however, did not contain similar organisms, and body part (i.e., the central capsule or the phaeodium) was the most important factor that divided the taxonomic composition of detected organisms, implying that the selection of appropriate body part is important when trying to ascertain contained organisms, even for unicellular zooplankton. Our results show that DNA metabarcoding on a single organism is effective in revealing the biological interactions of difficult-to-culture protists.     

Life history and environmental variation interact to determine effective population to census size ratio

Successful recovery and sustainability of threatened and exploited species depends in part on retention and maintenance of genetic diversity. Theory indicates that genetic diversity is lost at a rate inversely proportional to the genetically effective population size (N(e)), which is roughly equal to one-half the adult census size (N) in many organisms. However, N(e) has been reported to be up to five orders of magnitude lower than N in species with life histories that result in type III survivorship (high fecundity, but heavy mortality in early life stages, e.g. bony fishes), prompting speculation that low values of N(e) may be a general feature of such organisms despite sometimes vast abundances. Here, we compared N(e) and the ratio N(e)/N across three ecologically similar fish species from the arid southwestern United States, all with type III life histories but with differing expectations of egg and larval survivorship that correlate with the degree of human-imposed habitat fragmentation. Our study indicates that type III life history may be necessary, but this alone is insufficient to account for extraordinarily low values of N(e)/N. Rather, life history interacts with environmentally imposed mortality to determine the rate and magnitude of change in genetic diversity in these desert fish species.     

Translational selection shapes codon usage in the GC-rich genome of Chlamydomonas reinhardtii

In unicellular species codon usage is determined by mutational biases and natural selection. Among prokaryotes, the influence of these factors is different if the genome is skewed towards AT or GC, since in AT-rich organisms translational selection is absent. On the other hand, in AT-rich unicellular eukaryotes the two factors are present. In order to understand if GC-rich genomes display a similar behavior, the case of Chlamydomonas reinhardtii was studied. Since we found that translational selection strongly influences codon usage in this species, we conclude that there is not a common pattern among unicellular organisms.     

PCR Analysis of the Distribution of Unicellular Cyanobacterial Diazotrophs in the Arabian Sea

An oligonucleotide primer, NITRO821R, targeting the 16S rRNA gene of unicellular cyanobacterial N₂ fixers was developed based on newly derived sequences from Crocosphaera sp. strain WH 8501 and Cyanothece sp. strains WH 8902 and WH 8904 as well as several previously described sequences of Cyanothece sp. and sequences of intracellular cyanobacterial symbionts of the marine diatom Climacodium frauenfeldianum. This oligonucleotide is specific for the targeted organisms, which represent a well-defined phylogenetic lineage, and can detect as few as 50 cells in a standard PCR when it is used as a reverse primer together with the cyanobacterium- and plastid-specific forward primer CYA359F (U. Nübel, F. Garcia-Pichel, and G. Muyzer, Appl. Environ. Microbiol. 63:3327-3332, 1997). Use of this primer pair in the PCR allowed analysis of the distribution of marine unicellular cyanobacterial diazotrophs along a transect following the 67°E meridian from Victoria, Seychelles, to Muscat, Oman (0.5°S to 26°N) in the Arabian Sea. These organisms were found to be preferentially located in warm (>29°C) oligotrophic subsurface waters between 0 and 7°N, but they were also found at a station north of Oman at 26°N, 56°35′E, where similar water column conditions prevailed. Slightly cooler oligotrophic waters (<29°C) did not contain these organisms or the numbers were considerably reduced, suggesting that temperature is a key factor in dictating the abundance of this unicellular cyanobacterial diazotroph lineage in marine environments.     

Calnexin Delta 185-520 partially reverses the misprocessing of the Delta F508 cystic fibrosis transmembrane conductance regulator

We analyzed the interrelation between the efficiency of a gene expression and the nucleotide composition of all protein-coding sequences in 38 unicellular organisms whose complete genomic sequences are known. These organisms comprise 37 prokaryotic (29 eubacteria and eight archaebacteria) and one eukaryotic (yeast) species. We demonstrated that frequency analysis of gene codon composition fails to reflect adequately the gene expression efficiency of all these organisms. We constructed a measure, the elongation efficiency index, that considers simultaneously the information on codon frequencies and the degree of mRNA local self-complementarity. This measure recognizes the ribosome-coding genes as highly expressed in all the unicellular organisms studied. According to our analysis, these species fall into five groups differentiated by the process that makes the key contribution to the elongation rate.     

Evolution of complexity in the volvocine algae: transitions in individuality through Darwin's eye

The transition from unicellular to differentiated multicellular organisms constitutes an increase in the level complexity, because previously existing individuals are combined to form a new, higher-level individual. The volvocine algae represent a unique opportunity to study this transition because they diverged relatively recently from unicellular relatives and because extant species display a range of intermediate grades between unicellular and multicellular, with functional specialization of cells. Following the approach Darwin used to understand "organs of extreme perfection" such as the vertebrate eye, this jump in complexity can be reduced to a series of small steps that cumulatively describe a gradual transition between the two levels. We use phylogenetic reconstructions of ancestral character states to trace the evolution of steps involved in this transition in volvocine algae. The history of these characters includes several well-supported instances of multiple origins and reversals. The inferred changes can be understood as components of cooperation–conflict–conflict mediation cycles as predicted by multilevel selection theory. One such cycle may have taken place early in volvocine evolution, leading to the highly integrated colonies seen in extant volvocine algae. A second cycle, in which the defection of somatic cells must be prevented, may still be in progress.     

Initiation of self-organization processes in community of marine microbenthos by application of nutrients in super-high concentrations

The influence of high concentrations of mineral nitrogen, phosphorus and their mixtures on species structure of microbenthos of a sand intertidal zone of the White Sea was studies in field experiment. The increase in concentration of nutrients (in comparison with natural) reduces the species diversity and organism abundance in grazing chains, but stimulates the development of organisms of detrital food chain. At abnormally high concentration of nutrients the response of community does not strictly depend on chemical composition of fertilizers and N:P atomic ratio. The high concentration of nutrients act as distructive agent on the complex organized system and simultaneously as a specific trigger of self organization processes, which re resulted in formation of highly coherent commynity of r-strategists (bacteria and protists). After termination of the experiment and resetting of environment to the previous state, the new community for a long time (measured by dozens of generations of unicellular organisms) retains its structure.