Microbial systematics in the post-genomics era

Microbial systematics and phylogeny should form the foundation and guiding light for a comprehensive understanding of different aspects of microbiology. However, there are many critical issues in microbial systematics that are currently not resolved. Some of these include: how to define and delimit a prokaryotic species; development of rationale criteria for the assignment of higher taxonomic ranks; understanding what unique properties distinguish species from different groups; and understanding the branching order and interrelationship among higher prokaryotic clades. The sequencing of genomes from large numbers of cultured as well as uncultured microbes covering prokaryotic diversity provides unique means to achieve these important objectives. Prokaryotic genomes are found to be very diverse and dynamic and horizontal gene transfers (HGTs) are indicated to have played important role in species/genome evolution. Although HGT adds a layer of complexity in terms of understanding the genomes and species evolution, it is contended that vast majority of genes and genetic characteristics that are distinctive characteristics of higher prokaryotic taxa are vertically inherited and based on them a solid foundation for microbial systematics can be developed. We describe two kinds of molecular markers consisting of conserved indels in protein sequences and whole proteins that are specific for different groups that are proving particularly valuable in defining different prokaryotic groups in clear molecular terms and in understanding their interrelationships. The genetic and biochemical studies on these taxa-specific molecular markers also open the way to discover novel biochemical and physiological characteristics that are unique properties of these groups.     

Psychrophilic prokaryote structural-functional relationships, biogeography and evolution within marine sediment.

Prokaryote diversity has been found to be surprisingly high in cold marine sediments with numerous clades detected spread throughout many phyla. Marine benthic sediment clades are largely ecotypically distinct and autochthonous. Since almost all marine sediment prokaryotic taxa have yet to be cultivated, functionality is currently overwhelmingly cryptic for most benthic prokaryotic taxa except those falling into specific lineages for which there is cultivation or detailed biogeochemical data. Multivariate statistical comparisons of 16S rRNA gene sequence and denaturing gradient gel electrophoresis (DGGE) data show distinct distribution patterns of prokaryotic communities in sediment layers. By comparison geographical differences and differences related to the physical texture and organic content seem to result in generally smaller differences.     

Environmental distribution of prokaryotic taxa

Background  

The increasing availability of gene sequences of prokaryotic species in samples extracted from all kind of locations allows addressing the study of the influence of environmental patterns in prokaryotic biodiversity. We present a comprehensive study to address the potential existence of environmental preferences of prokaryotic taxa and the commonness of the specialist and generalist strategies. We also assessed the most significant environmental factors shaping the environmental distribution of taxa.     

环梅山岛海域春季浮游古菌群落空间分布特征研究

【目的】海洋浮游古菌是生物地球化学循环的关键驱动者,但其在近岸海域的水平空间分布特征还未被充分了解。本研究以与陆地紧密相连的环梅山岛海域为例研究浮游古菌在海陆过渡带的水平分布模式。【方法】利用16S rRNA基因扩增子测序,以期从优势类群分布、群落组成变化和物种共现模式3个层面揭示梅山湾潟湖区和临近海域春季浮游古菌的空间分布特征。【结果】该海域浮游古菌在原核生物群落中的相对丰度为0.6%–26.5%,向海侧古菌丰度显著高于潟湖区。浮游古菌群落由奇古菌门Marine Group(MG)I和广古菌门MGII主导,MGI的物种组成较为单一,而MGII的系统发育多样性较高。古菌群落的空间分布受同质扩散、环境选择和非主导过程(包括生态漂变)的共同塑造,其中环境选择主要由悬浮颗粒物、硝酸盐、溶解氧、水温和铵盐驱动。通过网络分析发现MGI与红杆菌科细菌呈广泛的负相关,MGII则普遍与SAR11、SAR116和SAR86等异养细菌类群呈正相关。【结论】本研究初步揭示了环梅山岛海域春季浮游古菌群落的空间分布特征及其调控因子,拓展了对古菌在海陆过渡带分布规律的认识。     

A call to arms for systematists: revitalising the purpose and practises underpinning the description of novel microbial taxa

Prokaryotic systematics is a fundamentally important discipline that provides a framework for the activities of all microbiologists. Here we propose that the field has become mired in a sea of perceived rules and regulations, many of which stipulate what is considered ‘sufficient’ for the phenotypic characterisation of novel prokaryotic taxa. Importantly, we argue also that the principles and practise of prokaryotic systematics have not yet fully embraced the revolution in biological understanding that has occurred through the availability of huge numbers of whole genome sequences. We therefore propose that a significant reappraisal of the procedures used to describe novel prokaryotic taxa is needed, including the likely introduction of new publication formats. Urgent action is needed to revitalise the practise of prokaryotic systematics in order to maintain this discipline as an attractive career choice for twenty first century life scientists.     

高于庄古生物学(英)

距今 14～ 16亿年的华北地区高于庄组黑色层状、结核状和透镜状燧石与叠层石的黑色硅质部分中保存着极丰富的原核和真核生物微化石。宏观藻类在该组的页岩中亦已发现。本组为评估中元古代生命状况、古环境和前显生宙生物地层提供了重要的生物信息。迄今为止在高于庄组地层中已有百余个化石种被人们认识。根据古植物和古环境的特征这些生物种类可分为三个不同的组合 ,即 :1.颤藻和色球藻组合 ,出现在高于庄组一段 ,代表浅水藻席建造者和居住者与一些可能的外来浮游生物的种类 ;2 .念珠藻组合 ,仅发生在该组的二段 ,还含一些底栖藻席建造者或居住者的种类 ;3.第四段的色球藻组合 ,它代表了潮间带至亚潮带的藻席建造者和外来的种类。元古代燧石中的微化石 ,尤其是蓝藻化石 ,尽管在元古代它们就已不断趋向于多样化 ,但由于它们形态上的保守性 ,对环境的指示比对地质时代的指示更有价值。高于庄组微化石的特点和大多数链状念珠藻垂直层理保存的事实表明 :1.高于庄组微化石的个体大小随时间趋向于增大 ;2 .高于庄组的沉积可能是处于一个淡水环境 ,且沉积率可能等于或少于微生物的生长率 ;3.高于庄组织沉积模式可能是从潮间带至亚潮带或深海 ,然后再至潮间带或潮上带 ;4 .当高于庄组沉积时真核生物亦已出现。     

Diatoms shape the biogeography of heterotrophic prokaryotes in early spring in the Southern Ocean

The interplay among microorganisms profoundly impacts biogeochemical cycles in the ocean. Culture-based work has illustrated the diversity of diatom–prokaryote interactions, but the question of whether these associations can affect the spatial distribution of microbial communities is open. Here, we investigated the relationship between assemblages of diatoms and of heterotrophic prokaryotes in surface waters of the Indian sector of the Southern Ocean in early spring. The community composition of diatoms and that of total and active prokaryotes were different among the major ocean zones investigated. We found significant relationships between compositional changes of diatoms and of prokaryotes. In contrast, spatial changes in the prokaryotic community composition were not related to geographic distance and to environmental parameters when the effect of diatoms was accounted for. Diatoms explained 30% of the variance in both the total and the active prokaryotic community composition in early spring in the Southern Ocean. Using co-occurrence analyses, we identified a large number of highly significant correlations between abundant diatom species and prokaryotic taxa. Our results show that key diatom species of the Southern Ocean are each associated with a distinct prokaryotic community, suggesting that diatom assemblages contribute to shaping the habitat type for heterotrophic prokaryotes.     

Prokaryotic evolution in light of gene transfer

Accumulating prokaryotic gene and genome sequences reveal that the exchange of genetic information through both homology-dependent recombination and horizontal (lateral) gene transfer (HGT) is far more important, in quantity and quality, than hitherto imagined. The traditional view, that prokaryotic evolution can be understood primarily in terms of clonal divergence and periodic selection, must be augmented to embrace gene exchange as a creative force, itself responsible for much of the pattern of similarities and differences we see between prokaryotic microbes. Rather than replacing periodic selection on genetic diversity, gene loss, and other chromosomal alterations as important players in adaptive evolution, gene exchange acts in concert with these processes to provide a rich explanatory paradigm-some of whose implications we explore here. In particular, we discuss (1) the role of recombination and HGT in giving phenotypic "coherence" to prokaryotic taxa at all levels of inclusiveness, (2) the implications of these processes for the reconstruction and meaning of "phylogeny," and (3) new views of prokaryotic adaptation and diversification based on gene acquisition and exchange.     

Quartet mapping and the extent of lateral transfer in bacterial genomes

Several recent analyses have used quartet-based methods to assess the congruence among phylogenies derived for large sets of genes from prokaryotic genomes. The principal conclusion from these studies is that lateral gene transfer (LGT) has blurred prokaryotic phylogenies to such a degree that the darwinian scheme of treelike evolution might be abandoned in favor of a net or web. Here, we focus on one of these methods, quartet mapping, and show that its application can lead to overestimation of the extent of inferred LGT in prokaryotes, particularly when applied to distantly related taxa.     

高于庄古生物学

距今14～16亿年的华北地区高于庄组黑色层状、结核状和透镜状燧石与叠层石的黑色硅质部分中保存着极丰富的原核和真核生物微化石.宏观藻类在该组的页岩中亦已发现.本组为评估中元古代生命状况、古环境和前显生宙生物地层提供了重要的生物信息.迄今为止在高于庄组地层中已有百余个化石种被人们认识.根据古植物和古环境的特征这些生物种类可分为三个不同的组合,即:1.颤藻和色球藻组合,出现在高于庄组一段,代表浅水藻席建造者和居住者与一些可能的外来浮游生物的种类;2.念珠藻组合,仅发生在该组的二段,还含一些底栖藻席建造者或居住者的种类;3.第四段的色球藻组合,它代表了潮间带至亚潮带的藻席建造者和外来的种类.元古代燧石中的微化石,尤其是蓝藻化石,尽管在元古代它们就已不断趋向于多样化,但由于它们形态上的保守性,对环境的指示比对地质时代的指示更有价值.高于庄组微化石的特点和大多数链状念珠藻垂直层理保存的事实表明:1.高于庄组微化石的个体大小随时间趋向于增大;2.高于庄组的沉积可能是处于一个淡水环境,且沉积率可能等于或少于微生物的生长率;3. 高于庄组织沉积模式可能是从潮间带至亚潮带或深海,然后再至潮间带或潮上带;4.当高于庄组沉积时真核生物亦已出现.     

Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology

Recent advances in the estimation of prokaryotic diversity have brought us insight into two questions: what is the extent of prokaryotic diversity, and perhaps more importantly, why bother finding out. In this review, we highlight the insights about the extent of diversity that may be gained by considering patterns that occur, or are likely to occur, in the relative abundance of prokaryotic taxa. We posit that global reservoirs of diversity are an important driving force behind patterns in localised diversity seen in leaves, intestines and wastewater treatment reactors. Thus, where the reservoir community is very large and relatively even, chance alone will prevent physically identical communities from having the same, or sometimes even stable, communities. By contrast, communities that tend to be similar (even when not physically identical) and stable are observed where the source diversity is low. Thus the relationship between structure and function in a community can only be understood, predicted and engineered through an understanding of the source of diversity from which the community is drawn.     

Major imprint of surface plankton on deep ocean prokaryotic structure and activity

Deep ocean microbial communities rely on the organic carbon produced in the sunlit ocean, yet it remains unknown whether surface processes determine the assembly and function of bathypelagic prokaryotes to a larger extent than deep‐sea physicochemical conditions. Here, we explored whether variations in surface phytoplankton assemblages across Atlantic, Pacific and Indian ocean stations can explain structural changes in bathypelagic (ca. 4,000 m) free‐living and particle‐attached prokaryotic communities (characterized through 16S rRNA gene sequencing), as well as changes in prokaryotic activity and dissolved organic matter (DOM) quality. We show that the spatial structuring of prokaryotic communities in the bathypelagic strongly followed variations in the abundances of surface dinoflagellates and ciliates, as well as gradients in surface primary productivity, but were less influenced by bathypelagic physicochemical conditions. Amino acid‐like DOM components in the bathypelagic reflected variations of those components in surface waters, and seemed to control bathypelagic prokaryotic activity. The imprint of surface conditions was more evident in bathypelagic than in shallower mesopelagic (200–1,000 m) communities, suggesting a direct connectivity through fast‐sinking particles that escape mesopelagic transformations. Finally, we identified a pool of endemic deep‐sea prokaryotic taxa (including potentially chemoautotrophic groups) that appear less connected to surface processes than those bathypelagic taxa with a widespread vertical distribution. Our results suggest that surface planktonic communities shape the spatial structure of the bathypelagic microbiome to a larger extent than the local physicochemical environment, likely through determining the nature of the sinking particles and the associated prokaryotes reaching bathypelagic waters.     

Microbial community diversity and composition varies with habitat characteristics and biofilm function in macrophyte‐rich streams

Biofilms in streams play an integral role in ecosystem processes and function yet few studies have investigated the broad diversity of these complex prokaryotic and eukaryotic microbial communities. Physical habitat characteristics can affect the composition and abundance of microorganisms in these biofilms by creating microhabitats. Here we describe the prokaryotic and eukaryotic microbial diversity of biofilms in sand and macrophyte habitats (i.e. epipsammon and epiphyton, respectively) in five macrophyte‐rich streams in Jutland, Denmark. The macrophyte species varied in growth morphology, C:N stoichiometry, and preferred stream habitat, providing a range in environmental conditions for the epiphyton. Among all habitats and streams, the prokaryotic communities were dominated by common phyla, including Alphaproteobacteria, Bacteriodetes, and Gammaproteobacteria, while the eukaryotic communities were dominated by Stramenopiles (i.e. diatoms). For both the prokaryotes and eukaryotes, the epipsammon were consistently the most diverse communities and the epiphytic communities were generally similar among the four macrophyte species. However, the communities on the least complex macrophyte, Sparganium emersum, had the lowest richness and evenness and fewest unique OTUs, whereas the macrophyte with the most morphological complexity, Callitriche spp., had the highest number of unique OTUs. In general, the microbial taxa were ubiquitously distributed across the relatively homogeneous Danish landscape as determined by measuring the similarity among communities (i.e. Sørensen similarity index). Furthermore, we found significant correlations between microbial diversity (i.e. Chao1 rarefied richness and Pielou's evenness) and biofilm structure and function (i.e. C:N ratio and ammonium uptake efficiency, respectively); communities with higher richness and evenness had higher C:N ratios and lower uptake efficiency. In addition to describing the prokaryotic and eukaryotic community composition in stream biofilms, our study indicates that 1) physical habitat characteristics influence microbial diversity and 2) the variation in microbial diversity may dictate the structural and functional characteristics of stream biofilm communities.     

Global diversity and biogeography of deep-sea pelagic prokaryotes

The deep-sea is the largest biome of the biosphere, and contains more than half of the whole ocean''s microbes. Uncovering their general patterns of diversity and community structure at a global scale remains a great challenge, as only fragmentary information of deep-sea microbial diversity exists based on regional-scale studies. Here we report the first globally comprehensive survey of the prokaryotic communities inhabiting the bathypelagic ocean using high-throughput sequencing of the 16S rRNA gene. This work identifies the dominant prokaryotes in the pelagic deep ocean and reveals that 50% of the operational taxonomic units (OTUs) belong to previously unknown prokaryotic taxa, most of which are rare and appear in just a few samples. We show that whereas the local richness of communities is comparable to that observed in previous regional studies, the global pool of prokaryotic taxa detected is modest (~3600 OTUs), as a high proportion of OTUs are shared among samples. The water masses appear to act as clear drivers of the geographical distribution of both particle-attached and free-living prokaryotes. In addition, we show that the deep-oceanic basins in which the bathypelagic realm is divided contain different particle-attached (but not free-living) microbial communities. The combination of the aging of the water masses and a lack of complete dispersal are identified as the main drivers for this biogeographical pattern. All together, we identify the potential of the deep ocean as a reservoir of still unknown biological diversity with a higher degree of spatial complexity than hitherto considered.     

Photoregulation in prokaryotes

The spectroscopic identification of sensory rhodopsin I by Bogomolni and Spudich in 1982 provided a molecular link between the light environment and phototaxis in Halobacterium salinarum, and thus laid the foundation for the study of signal transducing photosensors in prokaryotes. In recent years, a number of new prokaryotic photosensory receptors have been discovered across a broad range of taxa, including dozens in chemotrophic species. Among these photoreceptors are new classes of rhodopsins, BLUF-domain proteins, bacteriophytochromes, cryptochromes, and LOV-family photosensors. Genetic and biochemical analyses of these receptors have demonstrated that they can regulate processes ranging from photosynthetic pigment biosynthesis to virulence.     

Genetic diversity patterns of microbial communities in a subtropical riverine ecosystem (Jiulong River,southeast China)

Prokaryotic and eukaryotic microbes are key organisms in aquatic ecosystems and play pivotal roles in the biogeochemical cycles, but little is known about genetic diversity of these communities in subtropical rivers. In this study, microbial planktonic communities were determined by using denaturing gradient gel electrophoresis (DGGE) analysis from the Jiulong River, southeast China, and their relationships with local environmental factors were studied. The Betaproteobacteria (26%) and Dinophyceae (26%) were the most dominant taxa in prokaryotic and eukaryotic clones derived from DGGE bands, respectively. Further, both cluster and ordination analyses of prokaryotic and eukaryotic DGGE fingerprinting resulted in three identical groups from the 15 sites, which were closely related with the environmental factors. Partial redundancy analysis (partial RDA) revealed that agricultural pollution (phosphorus and nitrogen) and saltwater intrusion (conductivity and salinity) were the main factors impacting microbial community composition, by explaining more than two-thirds of the total variation in both prokaryotic (67.0%) and eukaryotic (70.5%) communities. Moreover, the robust and quantifiable relationship between DGGE results and environmental variables indicated that the community-level molecular fingerprinting techniques could support the physicochemical assessment of riverine water quality and ecosystem health.     

Diet Alters Both the Structure and Taxonomy of the Ovine Gut Microbial Ecosystem

We surveyed the ruminal metagenomes of 16 sheep under two different diets using Illumina pair-end DNA sequencing of raw microbial DNA extracted from rumen samples. The resulting sequence data were bioinformatically mapped to known prokaryotic 16S rDNA sequences to identify the taxa present in the samples and then analysed for the presence of potentially new taxa. Strikingly, the majority of the microbial individuals found did not map to known taxa from 16S sequence databases. We used a novel statistical modelling approach to compare the taxonomic distributions between animals fed a forage-based diet and those fed concentrated grains. With this model, we found significant differences between the two groups both in the dominant taxa present in the rumen and in the overall shape of the taxa abundance curves. In general, forage-fed animals have a more diverse microbial ecosystem, whereas the concentrate-fed animals have ruminal systems more heavily dominated by a few taxa. As expected, organisms from methanogenic groups are more prevalent in forage-fed animals. Finally, all of these differences appear to be grounded in an underlying common input of new microbial individuals into the rumen environment, with common organisms from one feed group being present in the other, but at much lower abundance.     

Protozoa populations are ecosystem engineers that shape prokaryotic community structure and function of the rumen microbial ecosystem

Unicellular eukaryotes are an integral part of many microbial ecosystems where they interact with their surrounding prokaryotic community—either as predators or as mutualists. Within the rumen, one of the most complex host-associated microbial habitats, ciliate protozoa represent the main micro-eukaryotes, accounting for up to 50% of the microbial biomass. Nonetheless, the extent of the ecological effect of protozoa on the microbial community and on the rumen metabolic output remains largely understudied. To assess the role of protozoa on the rumen ecosystem, we established an in-vitro system in which distinct protozoa sub-communities were introduced to the native rumen prokaryotic community. We show that the different protozoa communities exert a strong and differential impact on the composition of the prokaryotic community, as well as its function including methane production. Furthermore, the presence of protozoa increases prokaryotic diversity with a differential effect on specific bacterial populations such as Gammaproteobacteria, Prevotella and Treponema. Our results suggest that protozoa contribute to the maintenance of prokaryotic diversity in the rumen possibly by mitigating the effect of competitive exclusion between bacterial taxa. Our findings put forward the rumen protozoa populations as potentially important ecosystem engineers for future microbiome modulation strategies.Subject terms: Microbial ecology, Food webs