'Everything is everywhere: but the environment selects': ubiquitous distribution and ecological determinism in microbial biogeography

Recent discoveries of geographical patterns in microbial distribution are undermining microbiology's exclusively ecological explanations of biogeography and their fundamental assumption that 'everything is everywhere: but the environment selects'. This statement was generally promulgated by Dutch microbiologist Martinus Wilhelm Beijerinck early in the twentieth century and specifically articulated in 1934 by his compatriot, Lourens G. M. Baas Becking. The persistence of this precept throughout twentieth-century microbiology raises a number of issues in relation to its formulation and widespread acceptance. This paper will trace the conceptual history of Beijerinck's claim that 'everything is everywhere' in relation to a more general account of its theoretical, experimental and institutional context. His principle also needs to be situated in relationship to plant and animal biogeography, which, this paper will argue, forms a continuum of thought with microbial biogeography. Finally, a brief overview of the contemporary microbiological research challenging 'everything is everywhere' reveals that philosophical issues from Beijerinck's era of microbiology still provoke intense discussion in twenty-first century investigations of microbial biogeography.     

大数据时代土壤微生物地理学研究综述

土壤蕴含极为丰富的微生物多样性,它们在物质分解、元素生物地球化学循环、植物生产力和生物健康中扮演着关键角色。理解土壤微生物的生物地理分布格局、形成机制与群落构建规则,有助于预测在全球变化背景下土壤微生物组的功能演变及其对陆地生态系统的调控影响。自21世纪以来,土壤微生物生物地理学在各种大型国际微生物计划的推动下逐步形成了分子生物学技术耦合大数据分析的模式,实现了多种尺度上的关联研究。阐述了土壤微生物在分布格局和群落构建规则方面的研究进展,重点介绍了分子生物学技术和大数据分析在土壤微生物生物地理研究中的应用,对土壤微生物生物地理学未来在微生物分类分辨率、模型验证与构建和功能基因地理学的发展方向进行了展望。     

No biogeographical pattern for a root‐associated fungal species complex

Aim The biogeography of microbes is poorly understood and there is an open debate regarding if and how microbial biodiversity is structured. At the beginning of the 20th century, Baas Becking laid the foundations for the biogeography of microbes by stating that ‘Everything is everywhere, but the environment selects’ (the EisE hypothesis). This hypothesis remained dogma for almost a century. However, the recognition that microbial ‘species’ are often assemblages of reproductively isolated lineages challenged the EisE hypothesis, leading to the now common assumption that microbial communities possess cryptic biogeographic structures. We tested the presence of a cryptic biogeographical structure for a well‐characterized fungal species complex (the Phialocephala fortinii s.l.–Acephala applanata species complex, PAC) using precise molecular species resolution. In addition, we analysed factors that could govern PAC community assembling. Locations Forty‐four study sites in temperate and boreal forests across the Northern Hemisphere were included. Methods (1) The distance–decay relationship among PAC communities was calculated and a resampling procedure was applied to analyse the effect of sampling intensity and geographic distances among PAC communities. (2) Factors shaping PAC communities (e.g. climatic factors and tree species composition) were studied. (3) We tested PAC communities for random composition. Results We found that the similarity of species assemblages did not decrease with increasing geographical distance. Moreover, species diversity did not increase by expanding the area sampled. Instead, species diversity increased by increasing the sampling effort. Community composition correlated neither with tree species composition nor climate, and no association among species was observed. Main conclusions We could not discover any cryptic biogeographic structure even after applying refined species assignment but we demonstrate the importance of sampling effort for understanding the biogeography of microorganisms. Moreover, we show that primarily stochastic effects are responsible for the species composition of PAC communities.     

Synthesizing traditional biogeography with microbial ecology: the importance of dormancy

The discovery of biogeographical patterns among microbial communities has led to a focus on the empirical evaluation of the importance of dispersal limitation in microbial biota. As a result, the spatial distribution of microbial diversity has been increasingly studied while the synthesis of biogeographical theory with microbial ecology remains undeveloped. To make biogeographical theory relevant to microbial ecology, microbial traits that potentially affect the distribution of microbial diversity need to be considered. Given that many microorganisms in natural environments are in a state of dormancy and that dormancy is an important microbial fitness trait, I provide a first attempt to account for the effects of dormancy on microbial biogeography by treating dormancy as a fundamental biogeographical response. I discuss the effects of dormancy on the equilibrium theory of island biogeography and on the unified neutral theory of biodiversity and biogeography, and suggest how the equilibrium theory of island biogeography can produce predictions approaching those of the Baas‐Becking hypothesis (i.e. everything is everywhere, but the environment selects). In addition, I present a conceptual model of the unified neutral theory of biodiversity and biogeography, generalized to account for dormancy, from which a full model can be constructed for species with or without dormant life history stages.     

Microbial biogeography: putting microorganisms on the map

We review the biogeography of microorganisms in light of the biogeography of macroorganisms. A large body of research supports the idea that free-living microbial taxa exhibit biogeographic patterns. Current evidence confirms that, as proposed by the Baas-Becking hypothesis, 'the environment selects' and is, in part, responsible for spatial variation in microbial diversity. However, recent studies also dispute the idea that 'everything is everywhere'. We also consider how the processes that generate and maintain biogeographic patterns in macroorganisms could operate in the microbial world.     

土壤微生物生物地理学研究进展

生物地理学是研究生物（包括种群、群落等不同层次）地理分布格局及成因的一门交叉学科。微生物生物地理学的研究长期滞后于宏生物地理学。鉴于土壤微生物在调控生物地球化学过程和维持生态系统功能方面的重要作用,对其空间分布格局及形成机制的认识具有十分重要的理论和实际意义。随着分子生物学技术的发展,对微生物多样性的认知日益深入。越来越多的证据表明,土壤微生物群落结构和多样性具有一定的时空分布格局,从而对微生物全球性随机分布的传统观点提出了挑战。对当前土壤微生物生物地理学研究中的一些概念性问题,如微生物物种的定义、微生物多样性的定量测度、对微生物全球性随机分布的争论等,进行了系统评述;以微生物种-面积关系和距离-衰减关系为例对当前最新的土壤微生物生物地理学研究成果进行总结,并初步探讨了土壤微生物群落的地带性分布问题;在传统生物地理学理论的指导下,提出了一个可用于验证土壤微生物空间分布格局形成和机制维持的简单研究框架。这些对今后土壤微生物生物地理学的研究有一定借鉴和指导意义。     

Hybrids, pure cultures, and pure lines: from nineteenth-century biology to twentieth-century genetics

Prompted by recent recognitions of the omnipresence of horizontal gene transfer among microbial species and the associated emphasis on exchange, rather than isolation, as the driving force of evolution, this essay will reflect on hybridization as one of the central concerns of nineteenth-century biology. I will argue that an emphasis on horizontal exchange was already endorsed by 'biology' when it came into being around 1800 and was brought to full fruition with the emergence of genetics in 1900. The true revolution in nineteenth-century life sciences, I maintain, consisted in a fundamental shift in ontology, which eroded the boundaries between individual and species, and allowed biologists to move up and down the scale of organic complexity. Life became a property extending both 'downwards', to the parts that organisms were composed of, as well as 'upwards', to the collective entities constituted by the relations of exchange and interaction that organisms engage in to reproduce. This mode of thinking was crystallized by Gregor Mendel and consolidated in the late nineteenth-century conjunction of biochemistry, microbiology and breeding in agro-industrial settings. This conjunction and its implications are especially exemplified by Wilhelm Johannsen's and Martinus Beijerinck's work on pure lines and cultures. An understanding of the subsequent constraints imposed by the evolutionary synthesis of the twentieth century on models of genetic systems may require us to rethink the history of biology and displace Darwin's theory of natural selection from that history's centre.     

历史生物地理学进展

生物地理学研究动植物的地理分布。历史生物地理学重建生物区系历史。分替理论的复兴动摇了散布理论的上百年统治。最近10年主要是分替理论推动了历史生物地理学,出现了多个途径——种系发生物地理学、分支分替生物地理学、特有性的俭吝分析和泛生物地理学。岛屿生物地理学理论有了改进和严格的实验检验;庇所学说产生了新的模型。最后就我国如何发展生物地理学提出了对策措施。     

Diversity and biogeography of marine actinobacteria

The actinomycetes, although not all the Actinobacteria, are easy to isolate from the marine environment. However, their ecological role in the marine ecosystem is largely neglected and various assumptions meant there was little incentive to isolate strains for search and discovery of new drugs. However, the marine environment has become a prime resource in search and discovery for novel natural products and biological diversity, and marine actinomycetes turn out to be important contributors. Similarly, striking advances have been made in marine microbial ecology using molecular techniques and metagenomics, and actinobacteria emerge as an often significant, sometimes even dominant, environmental clade. Both approaches - cultivation methods and molecular techniques - are leading to new insights into marine actinobacterial biodiversity and biogeography. Very different views of actinobacterial diversity emerge from these, however, and the true extent and biogeography of this are still not clear. These are important for developing natural product search and discovery strategies, and biogeography is a hot topic for microbial ecologists.     

Biogeography and ecology: towards the integration of two disciplines

Although ecology and biogeography had common origins in the natural history of the nineteenth century, they diverged substantially during the early twentieth century as ecology became increasingly hypothesis-driven and experimental. This mechanistic focus narrowed ecology''s purview to local scales of time and space, and mostly excluded large-scale phenomena and historical explanations. In parallel, biogeography became more analytical with the acceptance of plate tectonics and the development of phylogenetic systematics, and began to pay more attention to ecological factors that influence large-scale distributions. This trend towards unification exposed problems with terms such as ‘community’ and ‘niche,’ in part because ecologists began to view ecological communities as open systems within the contexts of history and geography. The papers in this issue represent biogeographic and ecological perspectives and address the general themes of (i) the niche, (ii) comparative ecology and macroecology, (iii) community assembly, and (iv) diversity. The integration of ecology and biogeography clearly is a natural undertaking that is based on evolutionary biology, has developed its own momentum, and which promises novel, synthetic approaches to investigating ecological systems and their variation over the surface of the Earth. We offer suggestions on future research directions at the intersection of biogeography and ecology.     

Microbial diversity-productivity relationships in aquatic ecosystems

Thanks to recent advances in molecular biology, one's knowledge of microbial co-occurrence patterns, microbial biogeography and microbial biodiversity is expanding rapidly. This MiniReview explores microbial diversity-productivity relationships in the light of what is known from the general ecology literature. Analyses of microbial diversity-productivity relationships from 70 natural, experimental, and engineered aquatic ecosystems reveal patterns that are strikingly similar to those that have long been documented for communities of macroorganisms. Microbial ecology and the general science of ecology are thus continuing to converge.     

The Pareto principle: To what extent does it apply to resource acquisition in stable microbial communities and thereby steer their geno−/ecotype compositions and interactions between their members?

The Pareto principle, or 20:80 rule, describes resource distribution in stable communities whereby 20% of community members acquire 80% of a key resource. In this Burning Question, we ask to what extent the Pareto principle applies to the acquisition of limiting resources in stable microbial communities; how it may contribute to our understanding of microbial interactions, microbial community exploration of evolutionary space, and microbial community dysbiosis; and whether it can serve as a benchmark of microbial community stability and functional optimality?     

Beijerinck's work on tobacco mosaic virus: historical context and legacy

Beijerinck's entirely new concept, launched in 1898, of a filterable contagium vivum fluidum which multiplied in close association with the host's metabolism and was distributed in phloem vessels together with plant nutrients, did not match the then prevailing bacteriological germ theory. At the time, tools and concepts to handle such a new kind of agent (the viruses) were non-existent. Beijerinck's novel idea, therefore, did not revolutionize biological science or immediately alter human understanding of contagious diseases. That is how bacteriological dogma persisted, as voiced by Loeffler and Frosch when showing the filterability of an animal virus (1898), and especially by Ivanovsky who had already in 1892 detected filterability of the agent of tobacco mosaic but kept looking for a microbe and finally (1903) claimed its multiplication in an artificial medium. The dogma was also strongly advocated by Roux in 1903 when writing the first review on viruses, which he named 'so-called "invisible" microbes', unwittingly including the agent of bovine pleuropneumonia, only much later proved to be caused by a mycoplasma. In 1904, Baur was the first to advocate strongly the chemical view of viruses. But uncertainty about the true nature of viruses, with their similarities to enzymes and genes, continued until the 1930s when at long last tobacco mosaic virus particles were isolated as an enzyme-like protein (1935), soon to be better characterized as a nucleoprotein (1937). Physicochemical virus studies were a key element in triggering molecular biology which was to provide further means to reveal the true nature of viruses 'at the threshold of life'. Beijerinck's 1898 vision was not appreciated or verified during his lifetime. But Beijerinck already had a clear notion of the mechanism behind the phenomena he observed. Developments in virology and molecular biology since 1935 indicate how close Beijerinck (and even Mayer, Beijerinck's predecessor in research on tobacco mosaic) had been to the mark. The history of research on tobacco mosaic and the commitments of Mayer, Beijerinck and others demonstrate that progress in science is not only a matter of mere technology but of philosophy as well. Raemaekers' Mayer cartoon, inspired by Beijerinck, artistically represents the crucial question about the reliability of our images of reality, and about the scope of our technological interference with nature.     

Biogeographical patterns of soil molecular microbial biomass as influenced by soil characteristics and management

Aim The spatial organization of soil microbial communities on large scales and the identification of environmental factors structuring their distribution have been little investigated. The overall objective of this study was to determine the spatial patterning of microbial biomass in soils over a wide extent and to rank the environmental filters most influencing this distribution. Location French territory using the French Soil Quality Monitoring Network. This network covers the entire French territory and soils were sampled at 2150 sites along a systematic grid. Methods The soil DNA extracted from all these soils was expressed in terms of soil molecular microbial biomass and related to other soil and land‐use data over French territory. Results This study provides the first extensive map of microbial biomass and reveals the heterogeneous and spatially structured distribution of this biomass on the scale of France. The main factors driving biomass distribution are the physico‐chemical properties of the soil (texture, pH and total organic carbon) as well as land use. Soils from land used for intensive agriculture, especially monoculture and vineyards, exhibited the smallest biomass pools. Interestingly, factors known to influence the large‐scale distribution of macroorganisms, such as climatic factors, were not identified as important drivers for microbial communities. Main conclusions Microbial abundance is spatially structured and dependent on local filters such as soil characteristics and land use but is relatively independent of global filters such as climatic factors or the presence of natural barriers. Our study confirms that the biogeography of microorganisms differs fundamentally from the biogeography of ‘macroorganisms’ and that soil management can have significant large‐scale effects.     

世界樟科植物系统学研究进展

就上世纪 90年代以来世界樟科植物系统学研究进展 ,从形态学、孢粉学、胚胎学、叶角质层研究、分子系统学以及生物地理学等 6方面进行了综述性的回顾和展望     

How will bioinformatics influence metabolic engineering?

Ten microbial genomes have been fully sequenced to date, and the sequencing of many more genomes is expected to be completed before the end of the century. The assignment of function to open reading frames (ORFs) is progressing, and for some genomes over 70% of functional assignments have been made. The majority of the assigned ORFs relate to metabolic functions. Thus, the complete genetic and biochemical functions of a number of microbial cells may be soon available. From a metabolic engineering standpoint, these developments open a new realm of possibilities. Metabolic analysis and engineering strategies can now be built on a sound genomic basis. An important question that now arises; how should these tasks be approached? Flux-balance analysis (FBA) has the potential to play an important role. It is based on the fundamental principle of mass conservation. It requires only the stoichiometric matrix, the metabolic demands, and some strain specific parameters. Importantly, no enzymatic kinetic data is required. In this article, we show how the genomically defined microbial metabolic genotypes can be analyzed by FBA. Fundamental concepts of metabolic genotype, metabolic phenotype, metabolic redundancy and robustness are defined and examples of their use given. We discuss the advantage of this approach, and how FBA is expected to find uses in the near future. FBA is likely to become an important analysis tool for genomically based approaches to metabolic engineering, strain design, and development.     

Panbiogeography: Its origin,metamorphosis and decline

From the viewpoint of 2007, one can trace the history of an interesting and contentious trend in biogeography and evolution that began with Croizat’s concept of panbiogeography in 1958. After a quiescent period of about 16 years, some young biologists in New York and in New Zealand read Croizat’s books and became enthusiastic supporters of his ideas. In New York, in the early 1970s, panbiogeography was combined with a part of Hennig’s phylogenetic method to create vicariance biogeography. In 1986, the name of the latter was changed to cladistic biogeography. In the meantime, Croizat’s followers in New Zealand sought to maintain panbiogeography in its original form without reference to phylogeny. This idea reached its peak of popularity in 1989–1990 and then began to fade. In comparison, cladistic biogeography became much more widespread, especially when its followers began publishing laudatory books and papers. Its decline became noticeable after the turn of the century as the dispersal counterrevolution began to have its effect. It served a useful purpose by engaging the interest of young biologists who otherwise may not have become aware of biogeography.     

气温上升对草地土壤微生物群落结构的影响

在 2 0世纪内 ,全球气温已经上升了 0 .6℃ ,并预计到本世纪末仍将上升 1.4～ 5 .8℃。全球气候变暖对生态系统的潜在影响 ,生态系统对气温上升的反馈已成为国际生态学界的研究热点 ,而且所研究的系统也已经从过去简化的模拟系统到复杂的真实生态系统。但是 ,现有对真实生态系统的研究大部分集中在地上植物群落和土壤气体交换等领域 ,对在土壤有机碳分解和保护中起决定作用的土壤微生物研究较少。为此 ,在美国大平原地区进行人工提高气温 (上升 1.8℃ ) ,来研究土壤微生物对气温上升的反应。结果表明 :增温对土壤微生物的总生物量没有显著效应 ,但可以提高微生物的 C∶ N比。另外 ,磷脂肪酸分析发现 ,气温上升显著降低土壤微生物量中的细菌比重 ,提高真菌的份额 ,从而显著提高了群落中真菌与细菌的比值。而且 ,通过对土壤微生物底物利用方式和磷脂肪酸特征的主成份分析 ,发现增温导致了土壤微生物群落结构的转变。可见 ,气温上升可能是通过提高土壤微生物中真菌的优势 ,而导致群落结构的变化。该变化将可以提高微生物对土壤有机碳的利用效率 ,并利于土壤有机碳的保护     

Restricted distribution and limited gene flow in the model ciliate Tetrahymena thermophila

The biogeography of microbial eukaryotes has long been debated, but few phylogeographic data have been available to assess whether protists tend to have ubiquitous or endemic distributions. We addressed this issue in the ciliate Tetrahymena thermophila, a highly successful model system in cell and molecular biology. We found that this species has a distribution that is restricted to the Eastern United States, with high diversity in the northeast and low diversity across the rest of its distribution. We find high levels of population subdivision, low rates of migration and significant isolation by distance, supporting the moderate endemicity model of protist biogeography. This restricted gene flow may be a result of small population size, which would reduce the probability of migration events, or the inability to establish after migration. This work lays the foundation for T. thermophila to become a valuable model system for studying population biology.