Current debate on microbial diversity contrasts the 'cosmopolitan' hypothesis, which argues for high gene flow and low diversity, with the 'endemism' hypothesis, which argues for high diversity and geographically restricted gene flow. Our analyses of genetic variation in ciliate morphospecies isolated from ephemeral environments (freshwater ponds and tide pools) redefine this debate. In 2 different clades of oligotrich ciliates (in the genera Halteria/Meseres and Strombidium), we found both high levels of diversity and evidence of high gene flow as indicated by the presence of identical haplotypes across broad geographic ranges. Five recognizable morphospecies of Halteria/Meseres were found to be composed of 7 different clades, differing by as much as 7.6% sequence divergence at the ITS locus (ITS1, ITS2 and 5.8S rDNA). Two recognizable morphospecies of Strombidium (S. oculatum and S. stylifer) resolved into 10 distinct clades, differing by as much as 15.7% at the same locus. For both groups of ciliates, the genetic divergence underlying these morphospecies may be related to cycles of isolation in their ephemeral habitats (freshwater lakes and ponds for Halteria/Meseres and tide pools for Strombidium). By comparison, there is both low diversity and high gene flow in published data on ciliates from open coastal water (Laboea strobila and several species of tintinnids), a more stable environment over evolutionary time-scales. Our analyses indicate that models of microbial diversity must test for ecologically driven patterns in the interactions of gene flow and species richness to account for observed patterns of high dispersal and high gene flow.
SummaryBenthic microeukaryotes are key ecosystem drivers in marine sandy beaches, an important and dynamic environment; however, little is known about their diversity and biogeography on a large spatial scale. Here, we investigated the community composition and geographical distributions of benthic microeukaryotes using high-throughput sequencing of the 18S rRNA gene and quantified the contributions of environmental factors and spatial separation on the distribution patterns of both rare and abundant taxa. We collected 36 intertidal samples at 12 sandy beaches from four regions that spanned distances from 0.001 to 12,000 km. We found 12,890 operational taxonomic units (OTUs; 97% sequence identity level) including members of all eukaryotic super-groups and several phyla of uncertain position. Arthropoda and Diatomeae dominated the sequence reads in abundance, but Ciliophora and Discoba were the most diverse groups across all samples. About onethird of the OTUs could not be definitively classified at a similarity level of 80%, supporting the view that a large number of rare and minute marine species may have escaped previous characterization. We found generally similar geographical patterns for abundant and rare microeukaryotic sub-communities, and both showed a significant distance-decay similarity trend. Variation partitioning showed that both rare and abundant sub-communities exhibited a slightly stronger response to environmental factors than spatial (distance) factors. However, the abundant subcommunity was strongly correlated with variations in spatial, environmental and sediment grain size factors (66% of variance explained), but the rare assemblage was not (16%). This suggests that different or more complex mechanisms generate and maintain diversity in the rare biosphere in this habitat.
Planktonic ciliates within the subclasses Choreotrichia and Oligotrichia play critical roles in food webs in the world's oceans. To assess the diversity of these ciliates, we designed primers specific to small subunit ribosomal DNA (SSU rDNA) of ciliates within these clades and sampled at 3 coastal sites in the northwest Atlantic in October 2004 and May 2005. We also preserved and analyzed samples using standard ecological methods to compare observations from light microscopy with our molecular results. We found that (1) estimates of diversity based on molecular markers were similar to estimates from morphological observations for choreotrich ciliates, but much greater for oligotrich ciliates; (2) while similar levels of diversity were found at each site, each collection had its own distinct assemblage of rare and abundant ciliate haplotypes; (3) genealogical analyses of our samples combined with published sequences from identified morphospecies revealed that haplotype diversity at these sites is greatest within the genus Strombidium, in the Oligotrichia. The results from this ciliate-specific analysis are consistent with previous molecular studies on microbial diversity in marine systems in that they reveal high diversity and shifting assemblages within microbial communities.KEY WORDS: Ciliate phylogeography · Microzooplankton · Diversity · Oligotrichia · Choreotrichia · Strombidium · Culture independent Resale or republication not permitted without written consent of the publisherAquat Microb Ecol 48: [141][142][143][144][145][146][147][148][149][150][151][152][153][154] 2007 diverse assemblages within a genus, such as Strombidium spp. (Modigh 2001, Fileman & Leakey 2005. One exception is the tintinnids, a group of choreotrichs with a rich literature of morphological species descriptions based mainly on size and shape of the lorica (outer sheath). Ocean transect studies of tintinnid diversity reveal distinct assemblages within ocean provinces, with specific diversity patterns characterizing each area (Modigh et al. 2003, Thompson 2004. Further, compiling 451 data points from the literature for tintinnid diversity, Dolan et al. (2006) found a latitudinal distribution of tintinnid richness.Contemporary views on diversity of marine microbes have been altered by large-scale, molecular surveys (Caron et al. 2004, DeLong 2005, Giovannoni & Stingl 2005, Richards & Bass 2005, Xu 2006. Such studies revealed considerable microbial diversity not captured by culture-dependent methods. With these new methods, it is possible to sample from a broader range of microbial habitats (Dawson & Pace 2002, Edgcomb et al. 2002, Zettler et al. 2002, Lopez-Garcia et al. 2003, to sample previously undetected microbes (Diez et al. 2001, Moon-van der Staay et al. 2001, and to determine the spatial and temporal scales of microbial diversity (Romari & Vaulot 2004, Behnke et al. 2006, Cordova-Kreylos et al. 2006, Ley et al. 2006. Although ciliates are often captured in studies of eukaryotic diversity, we know of no published r...
To examine relationships among spirotrich ciliates using multi-locus sequence analyses and to provide preliminary insights into molecular diversity within species, we sequenced the small subunit rDNA (SSU rDNA), 5.8S rDNA, alpha-tubulin and the internally transcribed spacer regions (ITS1 and ITS2) of the rDNA genes from seven choreotrich (Class: Spirotrichea) and three oligotrich (Class: Spirotrichea) taxa. Genealogies constructed from SSU rDNA and ITS sequences are concordant and broadly support current classifications based on morphology. The one exception is the freshwater oligotrich Halteria grandinella, which, as has been previously noted, falls outside of the clade containing the other oligotrichs. In contrast, analyses of alpha-tubulin sequences are discordant with traditional taxonomy and rDNA genealogies. These analyses also indicate that considerably more genetic variation exists among choreotrich and oligotrich genera than among stichotrich genera. To explore the level of genetic variation among individuals in temporally isolated populations, we collected additional samples of a subset of planktonic choreotrichs and oligotrichs and characterized polymorphisms in ITS1, ITS2 and 5.8S rDNA. Analyses of these data indicate that, at least for some ciliate lineages, DNA polymorphisms vary temporally, and that genetic heterogeneity underlies some very similar morphological types.
This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40-60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on 'stolen' chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.
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