Where less may be more: how the rare biosphere pulls ecosystems strings

Rare species are increasingly recognized as crucial, yet vulnerable components of Earth’s ecosystems. This is also true for microbial communities, which are typically composed of a high number of relatively rare species. Recent studies have demonstrated that rare species can have an over-proportional role in biogeochemical cycles and may be a hidden driver of microbiome function. In this review, we provide an ecological overview of the rare microbial biosphere, including causes of rarity and the impacts of rare species on ecosystem functioning. We discuss how rare species can have a preponderant role for local biodiversity and species turnover with rarity potentially bound to phylogenetically conserved features. Rare microbes may therefore be overlooked keystone species regulating the functioning of host-associated, terrestrial and aquatic environments. We conclude this review with recommendations to guide scientists interested in investigating this rapidly emerging research area

Evolutionary Evidence of Algal Polysaccharide Degradation Acquisition by Pseudoalteromonas carrageenovora 9T to Adapt to Macroalgal Niches

About half of seaweed biomass is composed of polysaccharides. Most of these complex polymers have a marked polyanionic character. For instance, the red algal cell wall is mainly composed of sulfated galactans, agars and carrageenans, while brown algae contain alginate and fucose-containing sulfated polysaccharides (FCSP) as cell wall polysaccharides. Some marine heterotrophic bacteria have developed abilities to grow on such macroalgal polysaccharides. This is the case of Pseudoalteromonas carrageenovora 9T (ATCC 43555T), a marine gammaproteobacterium isolated in 1955 and which was an early model organism for studying carrageenan catabolism. We present here the genomic analysis of P. carrageenovora. Its genome is composed of two chromosomes and of a large plasmid encompassing 109 protein-coding genes. P. carrageenovora possesses a diverse repertoire of carbohydrate-active enzymes (CAZymes), notably specific for the degradation of macroalgal polysaccharides (laminarin, alginate, FCSP, carrageenans). We confirm these predicted capacities by screening the growth of P. carrageenovora with a large collection of carbohydrates. Most of these CAZyme genes constitute clusters located either in the large chromosome or in the small one. Unexpectedly, all the carrageenan catabolism-related genes are found in the plasmid, suggesting that P. carrageenovora acquired its hallmark capacity for carrageenan degradation by horizontal gene transfer (HGT). Whereas P. carrageenovora is able to use lambda-carrageenan as a sole carbon source, genomic and physiological analyses demonstrate that its catabolic pathway for kappa- and iota-carrageenan is incomplete. This is due to the absence of the recently discovered 3,6-anhydro-D-galactosidase genes (GH127 and GH129 families). A genomic comparison with 52 Pseudoalteromonas strains confirms that carrageenan catabolism has been recently acquired only in a few species. Even though the loci for cellulose biosynthesis and alginate utilization are located on the chromosomes, they were also horizontally acquired. However, these HGTs occurred earlier in the evolution of the Pseudoalteromonas genus, the cellulose- and alginate-related loci being essentially present in one large, late-diverging clade (LDC). Altogether, the capacities to degrade cell wall polysaccharides from macroalgae are not ancestral in the Pseudoalteromonas genus. Such catabolism in P. carrageenovora resulted from a succession of HGTs, likely allowing an adaptation to the life on the macroalgal surface

Multivariate Cutoff Level Analysis (MultiCoLA) of large community data sets

High-throughput sequencing techniques are becoming attractive to molecular biologists and ecologists as they provide a time- and cost-effective way to explore diversity patterns in environmental samples at an unprecedented resolution. An issue common to many studies is the definition of what fractions of a data set should be considered as rare or dominant. Yet this question has neither been satisfactorily addressed, nor is the impact of such definition on data set structure and interpretation been fully evaluated. Here we propose a strategy, MultiCoLA (Multivariate Cutoff Level Analysis), to systematically assess the impact of various abundance or rarity cutoff levels on the resulting data set structure and on the consistency of the further ecological interpretation. We applied MultiCoLA to a 454 massively parallel tag sequencing data set of V6 ribosomal sequences from marine microbes in temperate coastal sands. Consistent ecological patterns were maintained after removing up to 35–40% rare sequences and similar patterns of beta diversity were observed after denoising the data set by using a preclustering algorithm of 454 flowgrams. This example validates the importance of exploring the impact of the definition of rarity in large community data sets. Future applications can be foreseen for data sets from different types of habitats, e.g. other marine environments, soil and human microbiota

Marine protist diversity in European coastal waters and sediments as revealed by high-throughput sequencing

International audienceAlthough protists are critical components of marine ecosystems, they are still poorly characterized. Here we analysed the taxonomic diversity of planktonic and benthic protist communities collected in six distant European coastal sites. Environmental deoxyribonucleic acid (DNA) and ribonucleic acid (RNA) from three size fractions (pico-, nano- and micro/mesoplankton), as well as from dissolved DNA and surface sediments were used as templates for tag pyrosequencing of the V4 region of the 18S ribosomal DNA. Beta-diversity analyses split the protist community structure into three main clusters: picoplankton-nanoplankton-dissolved DNA, micro/mesoplankton and sediments. Within each cluster, protist communities from the same site and time clustered together, while communities from the same site but different seasons were unrelated. Both DNA and RNA-based surveys provided similar relative abundances for most class-level taxonomic groups. Yet, particular groups were overrepresented in one of the two templates, such as marine alveolates (MALV)-I and MALV-II that were much more abundant in DNA surveys. Overall, the groups displaying the highest relative contribution were Dinophyceae, Diatomea, Ciliophora and Acantharia. Also, well represented were Mamiellophyceae, Cryptomonadales, marine alveolates and marine stramenopiles in the picoplankton, and Monadofilosa and basal Fungi in sediments. Our extensive and systematic sequencing of geographically separated sites provides the most comprehensive molecular description of coastal marine protist diversity to date

Diversity and dynamics of rare and of resident bacterial populations in coastal sands

Coastal sands filter and accumulate organic and inorganic materials from the terrestrial and marine environment, and thus provide a high diversity of microbial niches. Sands of temperate climate zones represent a temporally and spatially highly dynamic marine environment characterized by strong physical mixing and seasonal variation. Yet little is known about the temporal fluctuations of resident and rare members of bacterial communities in this environment. By combining community fingerprinting via pyrosequencing of ribosomal genes with the characterization of multiple environmental parameters, we disentangled the effects of seasonality, environmental heterogeneity, sediment depth and biogeochemical gradients on the fluctuations of bacterial communities of marine sands. Surprisingly, only 3–5% of all bacterial types of a given depth zone were present at all times, but 50–80% of them belonged to the most abundant types in the data set. About 60–70% of the bacterial types consisted of tag sequences occurring only once over a period of 1 year. Most members of the rare biosphere did not become abundant at any time or at any sediment depth, but varied significantly with environmental parameters associated with nutritional stress. Despite the large proportion and turnover of rare organisms, the overall community patterns were driven by deterministic relationships associated with seasonal fluctuations in key biogeochemical parameters related to primary productivity. The maintenance of major biogeochemical functions throughout the observation period suggests that the small proportion of resident bacterial types in sands perform the key biogeochemical processes, with minimal effects from the rare fraction of the communities

Where less may be more: how the rare biosphere pulls ecosystems strings

Rare species are increasingly recognized as crucial, yet vulnerable components of Earth’s ecosystems. This is also true for microbial communities, which are typically composed of a high number of relatively rare species. Recent studies have demonstrated that rare species can have an over-proportional role in biogeochemical cycles and may be a hidden driver of microbiome function. In this review, we provide an ecological overview of the rare microbial biosphere, including causes of rarity and the impacts of rare species on ecosystem functioning. We discuss how rare species can have a preponderant role for local biodiversity and species turnover with rarity potentially bound to phylogenetically conserved features. Rare microbes may therefore be overlooked keystone species regulating the functioning of host-associated, terrestrial and aquatic environments. We conclude this review with recommendations to guide scientists interested in investigating this rapidly emerging research area

Ecological coherence of diversity patterns derived from classical fingerprinting and Next Generation Sequencing techniques

Changes in richness and bacterial community structure obtained via 454 Massively Parallel Tag Sequencing (MPTS) and Automated Ribosomal Intergenic Analysis (ARISA) were systematically compared to determine whether and how the ecological knowledge obtained from both molecular techniques could be combined. We evaluated community changes over time and depth in marine coastal sands at different levels of taxonomic resolutions, sequence corrections and sequence abundances. Although richness over depth layers or sampling dates greatly varied [∼ 30% and 70–80% new operational taxonomic units (OTU) between two samples with ARISA and MPTS respectively], overall patterns of community variations were similar with both approaches. Alpha-diversity estimated by ARISA-derived OTU was most similar to that obtained from MPTS-derived OTU defined at the order level. Similar patterns of OTU replacement were also found with MPTS at the family level and with 20–25% rare types removed. Using ARISA or MPTS datasets with lower resolution, such as those containing only resident OTU, yielded a similar set of significant contextual variables explaining bacterial community changes. Hence, ARISA as a rapid and low-cost fingerprinting technique represents a valid starting point for more in-depth exploration of community composition when complemented by the detailed taxonomic description offered by MPTS

Ecosystem-specific microbiota and microbiome databases in the era of big data

The rapid development of sequencing methods over the past decades has accelerated both the potential scope and depth of microbiota and microbiome studies. Recent developments in the field have been marked by an expansion away from purely categorical studies towards a greater investigation of community functionality. As in-depth genomic and environmental coverage is often distributed unequally across major taxa and ecosystems, it can be difficult to identify or substantiate relationships within microbial communities. Generic databases containing datasets from diverse ecosystems have opened a new era of data accessibility despite costs in terms of data quality and heterogeneity. This challenge is readily embodied in the integration of meta-omics data alongside habitat-specific standards which help contextualise datasets both in terms of sample processing and background within the ecosystem. A special case of large genomic repositories, ecosystem-specific databases (ES-DB’s), have emerged to consolidate and better standardise sample processing and analysis protocols around individual ecosystems under study, allowing independent studies to produce comparable datasets. Here, we provide a comprehensive review of this emerging tool for microbial community analysis in relation to current trends in the field. We focus on the factors leading to the formation of ES-DB’s, their comparison to traditional microbial databases, the potential for ES-DB integration with meta-omics platforms, as well as inherent limitations in the applicability of ES-DB’s