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Jiwen Liu, Zhe Meng, Xiaoyue Liu, Xiao-Hua Zhang. 2019: Microbial assembly, interaction, functioning, activity and diversifcation: a review derived from community compositional data. Marine Life Science & Technology, 1(1): 112-128. DOI: 10.1007/s42995-019-00004-3
Citation: Jiwen Liu, Zhe Meng, Xiaoyue Liu, Xiao-Hua Zhang. 2019: Microbial assembly, interaction, functioning, activity and diversifcation: a review derived from community compositional data. Marine Life Science & Technology, 1(1): 112-128. DOI: 10.1007/s42995-019-00004-3

Microbial assembly, interaction, functioning, activity and diversifcation: a review derived from community compositional data

  • Corresponding author:

    Xiao-Hua Zhang xhzhang@ouc.edu.cn

  • Received Date: 2019-03-26
  • Accepted Date: 2019-08-12
  • Published online: 2019-10-08
    Edited by Chengchao Chen.
  • Microorganisms play crucial roles in maintaining ecosystem stability. The last two decades have witnessed an upsurge in studies on marine microbial community composition using high-throughput sequencing methods. Extensive mining of the compositional data has provided exciting new insights into marine microbial ecology from a number of perspectives. Both deterministic and stochastic processes contribute to microbial community assembly but their relative importance in structuring subcommunities,that are categorized by traits such as abundance,functional type and activity,difers. Through correlation-based network analysis,signifcant progress has been made in unraveling microbial co-occurrence patterns and dynamics in response to environmental changes. Prediction of ecosystem functioning,based on microbial data,is receiving increasing attention,as closely related microbes often share similar ecological traits and microbial diversity often exhibits signifcant correlations to ecosystem functioning. The ecosystem functioning is likely executed not by the whole community,but rather by an active fraction of a community,which can be inferred from the marker gene transcription level of community members. Furthermore,the huge amount of microbial community data has signifcantly expanded the tree of life and illuminated microbial phylogenetic divergence and evolutionary history. This review summarizes important fndings in microbial assembly,interaction,functioning,activity and diversifcation,highlighting the interacting roles of diferent aspects,derived from community compositional data.
  • Microorganisms play key roles in biogeochemical cycling that are fundamental in maintaining climate and ecosystem stability. The structure of microbial communities is closely associated with environmental conditions and therefore is likely to evolve in the context of global change (Gutknecht et al. 2012). In the marine environment, frequent natural events and increasing human activity dramatically infuence microbial community dynamics, which will change the balance of biogeochemical cycles and alter ecosystem functioning (Hutchins and Fu 2017). One of the major concerns associated with global changes is how to efectively predict variations in ecosystem functioning. Microorganisms, as major drivers of many biogeochemical processes, provide a linkage between ecosystem functioning and environments (Singh et al. 2010).

    Marine microbial communities are signifcantly afected by environmental changes. Sanger and high-throughput sequencing in recent decades have provided an enormous amount of sequence data of molecular marker genes, including the ribosomal RNA (rRNA) gene. These data have helped to provide insights into marine microbial community dynamics (Liu et al. 2019; Needham et al. 2017; Reji et al. 2019), which are driven by environmental factors, such as salinity (Lozupone and Knight 2007) and temperature (Sunagawa et al. 2015). However, the association between environments and microbial dynamics (termed as deterministic processes) can be confounded by the efects of random events (termed as stochastic processes that include ecological drift and dispersal) (Mo et al. 2018; Wang et al. 2019; Zhou and Ning 2017). Deterministic and stochastic processes, which jointly determine microbial biogeography, vary in their relative contribution to community assembly over diferent temporal and spatial scales (Zhou and Ning 2017). Diferences in microbial distribution impact ecosystem functioning. Their relationships can mostly be explained by the observed correlations between microbial phylogeny and functional traits and between microbial diversity and ecosystem functioning. There are ways to predict microbial functional potential based on taxonomy (Aßhauer et al. 2015; Langille et al. 2013; Louca et al. 2016). Therefore, it has become increasingly common to improve the ftness of ecosystem functioning prediction by including microbial data.

    Marine microbes are highly diverse and encompass taxonomically and functionally diferent lineages. Complex interactions occur among microbial taxa, which underpin community stability and functioning. However, elucidation of microbial interactions is challenging and is largely dependent on correlation-based network analysis (Liu et al. 2014b; Milici et al. 2016; Zhang et al. 2014; Zhou et al. 2018). Diverse microbial communities can be divided into subcommunities, based on diferent criteria, such as abundance (abundant and rare taxa), functional type (e.g., autotrophic and heterotrophic taxa) and activity (active and dormant taxa). Accumulating evidence is showing that microbial subcommunities difer in their environmental sensitivity, interaction and distribution patterns (Wu et al. 2017; Zhang et al. 2014). Thus, diferent subcommunities may represent diferent consortiums and difer in their roles in ecosystem functioning prediction. Currently, the ecology of microbial subcommunities is less understood than the whole community, raising the need for a resolved community-based classifcation for future analysis.

    By implementing rRNA gene-based amplicon sequencing, numerous previously unknown microbial lineages, even at the phylum level, have been described from the marine environment (Brown et al. 2015; DeLong 1992; Inagaki et al. 2003). These, together with those identifed from terrestrial habitats, dramatically expand the tree of life (Hug et al. 2016). Refned phylogenetic analysis of molecular marker genes further demonstrates the occurrence of habitat-specifc ecotypes within a lineage (Ivars-Martinez et al. 2008; Liu et al. 2014a). The diversifcation of microorganisms can be attributed to a joint efect of genetic and environmental variabilities, which dictate the specifc evolutionary history of a taxon.

    In this review, five aspects are presented (microbial assembly, interaction, functioning, activity and diversifcation) to show how microbial community data contribute to the understanding of marine microbial ecology. They are organized along a stepwise understanding of the role microbial communities play in marine ecosystems. A synthetic view of these aspects will provide novel insights into their interactions and complementarity, which will in turn help to stimulate new ideas on the interpretation of community compositional data and the perception of new microbial community studies.

    One long debated question in community ecology is which processes determine an ecological community to assemble (Preston 1948). The current, well-established theories are primarily derived from research on animals and plants. Studies on microorganisms are scarce because of the assumption that microorganisms do not have distribution patterns due to their large numbers and small size (Baas-Becking 1934). However, using advanced sequencing technologies and statistical methods, microbial distribution patterns have been discovered in many natural environments including seawater and marine sediments (Liu et al. 2014b, 2015a; Lozupone and Knight 2007; Martiny et al. 2006). The spatial turnover of microbial communities always refects a distance-decay relationship and/or a taxa-area relationship, which are the two most well established patterns depicting increasing community dissimilarity with spatial distance (Nekola and White 1999) and increasing taxa richness with area size (Horner-Devine et al. 2004), respectively.

    A framework has been established that considers the niche and neutral theories as potential mechanisms underpinning microbial biogeography (Dini-Andreote et al. 2015; Dumbrell et al. 2010; Leibold and McPeek 2006; Table 1). The long standing niche theory shows how biodiversity is structured by physiochemical (environmental heterogeneity) and biotic (inter taxa interaction) factors (Chase and Leibold 2003). In niche theory, every taxon is assumed to have unique and non-overlapping traits, which enable it to exert diferent responses/efects on an environment and to occupy diferent ecological niches (Leibold 1995). This heterogeneity in traits also eliminates inter taxa competition by resource partition and thus allows an infnite number of taxa to coexist in an environment, leading to high microbial diversity (Leibold and McPeek 2006). In this context, niche theory cannot explain the observed diferences in the abundance of diferent taxa, although microbial abundance under niche theory always follows a log-normal distribution pattern (Hubbell 2001). Later, Hubbell (2001) proposed a neutral ecological view on the assembly of taxa-rich communities that consisted of many rare taxa. Unlike niche theory, the neutral theory assumes that all individuals are ecologically equivalent, share the same way of life and have a similar response/efect on environments. Therefore, interactions among microbes, and between microbes and environments are ignored in the neutral theory (Hubbell 2001). Microbial diversity is controlled by randomly occurring events, such as ecological drift (change in the relative abundance of taxa in a location due to chance demographic fuctuations) and dispersal (movement of taxa across spaces) (Chave 2004; Hanson et al. 2012; Hubbell 2001). Because such ecological events happen diferently to each individual taxon, the relative abundance of diferent taxa can be partially explained by the neutral theory (Volkov et al. 2003).

    Table  1.  Comparison of the niche and neutral theories
    The niche theory The neutral theory
    Time proposed 1959 (A general description of niche concept) 2001
    Concept Coexistence by niche diferentiation Random events occurring on individual taxon
    Traits Functionally diferent Functionally equivalent
    Relative abundance Log-normal distribution Zero-sum multinomial distribution
    Processes Abiotic environmental selection and biotic interspecifc interactions Ecological drift and dispersal
    Feature of process Deterministic Stochastic
     | Show Table
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    Microbial ecology studies have consistently considered abiotic selection as a niche-based (deterministic) process (also known as habitat flters or species sorting) and ecological drift and dispersal limitation as neutral-based (stochastic) processes (Fig. 1). Selections are mostly represented by environmental correlations. Drift is difcult to measure and it often interacts with restricted dispersal (dispersal limitation) to produce a distance-decay relationship (Hanson et al. 2012). Dispersal limitation is often represented by spatial distance. However, spatial distance can be a deterministic factor when it correlates to physiochemical factors and both population size (neutral) and traits (niche) can afect the dispersal ability of diferent taxa (Hanson et al. 2012). These make the relationships between selection, dispersal and stochasticity complex (Evans et al. 2017). To accurately evaluate stochasticity, neutral and null models have been increasingly implemented (Chase and Myers 2011; Jeraldo et al. 2012, Table 2). Nevertheless, these models cannot distinguish diferent aspects of the stochastic process. To solve this problem, Stegen et al.(2013, 2015) proposed a framework to quantify the relative roles of deterministic and stochastic processes. This framework integrates both the null model and phylogenetic information and assumes that phylogenetically close taxa tend to have similar ecological traits. It contains two steps with the frst to estimate the role of selection using phylogenetic dissimilarities and the second to diferentiate the role of dispersal and drift using the Bray–Curtis dissimilarities among microbial communities (Jia et al. 2018; Logares et al. 2018; Stegen et al. 2013, 2015; Zhou and Ning 2017).

    Figure  1.  The assembly of microbial communities is governed by a joint efect of deterministic (niche) and stochastic (neutral) processes. Subdivision of a microbial community (according to abundance, activity, function and occupancy) into subcommunities will facilitate an accurate view of microbial assembling processes
    Table  2.  Examples of studies examining the relative role of deterministic and stochastic processes in structuring microbial community
    Community Ecosystem Spatial scale Stochasticity measurement Relative importance References
    Determinism Stochasticity
    Terrestrial ecosystem
    Arbuscular mycorrhizal fungi Soil < 50 m Species relative abundance and spatial distance Dumbrell et al.(2010)
    Bacteria Desert Global Neutral model Heterotrophic community Photosynthetic community Caruso et al. (2011)
    Bacteria Freshwater lakes ~130 km in maximum Neutral community model Roguet et al. (2015)
    Bacteria Soil spanning 105 years succession Newly designed model Community when succession proceeded Community at initial stage Dini-Andreote et al.(2015)
    Bacteria and archaea Groundwater Stegen's framework Graham et al.(2017)
    Marine ecosystem
    Microbial eukaryotes Coastal water and sediment ~ 20 km in maximum Neutral community model and variation partitioning Chen et al. (2017)
    Bacteria Coastal water ~200 km Stegen's framework High eutrophication Low eutrophication Dai et al. (2017)
    Bacteria and protist Seawater 51–826 km Stegen's framework and variation partitioning Protist community(bottom water) Protist (surface and deep chlorophyll maximum waters) and bacterial (all three layers) communities Wu et al. (2018)
    Bacteria Coastal water ~1300 km in maximum Neutral model and variation partitioning Both abundant and rare communities Mo et al. (2018)
    Archaea Coastal water ~200 km Stegen's framework and variation partitioning Wang et al. (2019)
     | Show Table
    DownLoad: CSV

    Deterministic and stochastic processes jointly govern the assembly of microbial communities (Chave 2004). However, their relative importance varies across diferent spatial and temporal scales (Table 2), depending on the strength of environmental gradients and the sensitivity of the microbes to environmental changes. If the extent of environmental variation is greater than the threshold a microbe can endure, dispersal will be prevented (Wang et al. 2013), leading to the predominance of determinism. Thus, the mechanisms underlying microbial community assembly would alter over a seasonal or longer term period with changes in the magnitude of environmental heterogeneity (Dini-Andreote et al. 2015; Langenheder et al. 2012). These conclusions are mostly based on investigations of terrestrial microbial communities. By comparison, there have been very few studies on the relative roles of deterministic and stochastic processes in the marine environment. However, there is a general perception that stochastic processes have a greater efect on the assembly of planktonic bacterial and archaeal communities than deterministic processes (Table 2). This can be explained by marine prokaryotes having evolved strong adaptation capabilities to environmental changes and by spatial connectivity and seawater movement homogenizing environmental conditions. Another explanation is that the environmental factors analyzed to represent deterministic processes may be not the most relevant ones afecting community variations. Further studies are needed to confrm such a hypothesis and to compare the assembling processes between diferent habitats, such as coastal water vs open ocean and water vs sediment.

    Different types of marine organisms differ in their responses to deterministic and stochastic processes. Wu et al. (2018) reported that determinism had a stronger efect on planktonic protist communities than on bacterial communities, which may relate to diferences in their environmental sensitivity. Such diferent responses between bacteria and micro-eukaryotes have also been observed in soil (Powell et al. 2015a) and freshwater (Logares et al. 2018) habitats. Additionally, subcommunities that are divided by abundance, activity, functional trait or occupancy, can also undergo diferent ecological processes (Fig. 1). A microbial community is usually made up of a few abundant taxa and a long tail of rarer ones (Pedrós-Alió 2006, 2012). The rare taxa account for a great proportion of the microbial diversity and have been shown to assemble non-randomly and display similar distribution patterns to the abundant taxa (Galand et al. 2009; Gong et al. 2015; Liu et al. 2015b; Mo et al. 2018). Nevertheless, the abundant and rare taxa have both been observed to be diferently afected by stochastic and deterministic processes (Liu et al. 2015b; Mo et al. 2018). Mo et al. (2018) reported that the rare bacterioplankton in coastal seawater had a weaker response to environmental factors than abundant taxa; this may be due to the small population size of the rare taxa, making them more susceptible to ecological drift (Nemergut et al. 2013). By contrast, a survey of bacterial communities in freshwater lakes and reservoirs revealed a greater infuence of environmental changes on the rare than the abundant taxa (Liu et al. 2015b). These fndings suggest complicated microbial ecological responses across distinct ecosystems. In this context, further studies are needed to gain an insight into the assembling processes of abundant and rare taxa in different environments. The most urgent need is to propose a common defnition for rare taxa, facilitating a parallel comparison across studies (Jia et al. 2018). Subcommunities divided by functional traits, activity and occupancy receive less attention and have mainly been analyzed in terrestrial environments. For example, in deserts, the phototrophic community was mainly afected by stochastic processes, whereas the heterotrophic community displayed patterns mainly driven by environmental stresses (Caruso et al. 2011). The assembly of generalists and specialists in plateau lakes, however, was driven by stochastic and deterministic processes, respectively (Liao et al. 2016). While these studies provide novel and accurate information about the distribution patterns and assembling processes of microbial communities, there is an urgent need to investigate diferent subcommunities in the marine environment. It should be noticed that when evaluating the relative role of determinism and stochasticity, the estimated contribution from determinism is largely afected by the set of environmental factors measured, since they are not necessarily the most relevant parameters that provide the best explanatory power for the community variations.

    In niche theory, the microbe-microbe interactions, although being ecologically important, are less understood compared to the microbe-environment relationships (Chase and Leibold 2003). Inclusion of interactions to explain microbial distribution patterns is a great challenge, largely due to the difculty in obtaining microbial co-cultures. An alternative way of elucidating microbial interactions is to apply correlation-based network analysis (Barberán et al. 2012; Layeghifard et al. 2017; Weiss et al. 2016), which is enhanced by the increase of community compositional data and the development of statistical tools. The most popular method used for constructing a correlation-based network is to calculate the Spearman's rank correlation coefcients between taxa (Barberán et al. 2012; Table 2). Other methods are also available, including SPIEC-EASI, CCLasso, REBACCA, CoNet, SparCC, WGCNA, Molecular Ecological Networks Analysis, Local Similarity Analysis, Maximal Information Coefcient, etc. These methods, however, vary in their sensitivity and precision (Layeghifard et al. 2017; Weiss et al. 2016).

    Nodes and edges are fundamental components of a network, representing taxa and correlations, respectively. Edge thickness often denotes the degree of a correlation, with a thicker edge representing a higher correlation coefcient. On the basis of nodes and edges, a number of parameters can be calculated to represent the topological structure of a network, including degree, density, betweenness centrality, network diameter and clustering coefcient (Newman 2003). The degree of a node describes its connectivity to other nodes, with a higher value indicating a wider correlation. The betweenness centrality of a node describes the number of shortest paths between any two nodes going through it. The nodes with high degree and low betweenness centrality potentially represent the keystone taxa of a community (Berry and Widder 2014; Liang et al. 2016). The keystone taxa are the cornerstone and initial components for a community to assemble (Berry and Widder 2014) and have recently been defned as "highly connected taxa that individually or in a guild exert a considerable infuence on microbiome structure and functioning irrespective of their abundance across space and time" (Banerjee et al. 2018). A group of densely connected nodes with weak correlations to other nodes forms a module. Modular analysis can help to simplify the processes of identifying keystone taxa and/ or exploring the efect of environmental factors on microbemicrobe interactions.

    Despite having the potential to infer mutualistic (positive) and antagonistic (negative) efects, the co-occurrence patterns illustrated by the network analysis can have diferent meanings, such as similar environmental preference and lifestyle, resource partitioning and nutrient cross-feeding that do not involve direct interactions. Network analyses have consistently revealed patterns dominated by positive cooccurrences in both terrestrial and marine bacterial communities (Barberán et al. 2012; Ju et al. 2014; Liu et al. 2014b; Ma et al. 2016; Milici et al. 2016; Zhang et al. 2014; Zhou et al. 2018). This suggests a ubiquitous non hostile process in bacterial community assembling irrespective of habitat. In fact, a network analysis of prokaryotic communities in global surface seawater samples (Tara oceans) showed that positive co-occurrences accounted for up to 90% of all correlations (Lima-Mendez et al. 2015; Milici et al. 2016). This may be explained by the similar environmental preference (possibly driven by some unknown/unmeasured environmental factors) and/or high resistance of marine prokaryotes to environmental stresses, which enable them to coexist in the same ecological niche. Indeed, the fnding is in line with the observation of a relatively weaker efect of determinism relative to stochasticity on the distribution of marine planktonic prokaryotes as stated above. It is also likely that auxotrophy in marine microbes contributes to the observed positive correlations, since several bacterial groups (such as the SAR11 clade of Alphaproteobacteria, Tripp et al. 2009) have been observed to gain ftness by obtaining a biomolecule from other groups. By contrast, a study of planktonic bacterial communities in the South China Sea showed that negative correlations dominated the co-occurrence patterns in active bacteria compared to positive correlations in total bacteria (Zhang et al. 2014). Resource competition may occur in diferent active bacterial groups. It is noticeable that microbial networks vary with space and time (Table 3). Signifcant changes in network topological structures have been observed in seawater at diferent depths (Chow et al. 2013) and between diferent seasons (Chafee et al. 2018). Additionally, Milici et al. (2016) reported that free-living bacterioplankton possessed highly interconnected networks compared to particle-attached communities. They postulated that the distinct nutrient-utilizing strategies of these two groups might be responsible for such a discrepancy. However, it is unexpected to fnd more between-taxa connections in the free-living community, since particle-attached microbes have a higher cell abundance and are physically closer to one another. This provides further evidence that the network-derived co-occurrence patterns are not always good proxies of true interactions between microbes.

    Table  3.  Examples of network analysis conducted in the marine ecosystem
    Community Ecosystem Infuential factors Statistical methods References
    Network within a single system
    Bacteria and archaea Sediment Spearman's rank correlations Liu et al. (2014b)
    Bacteria Sediment Whittaker's index of associations Buttigieg and Ramette (2015)
    Bacteria Seawater WGCNA Bryant et al. (2016)
    Bacteria Sediment Spearman's rank correlations Qiao et al. (2018)
    Bacteria, archaea and microbial eukaryotes Seawater Spearman's rank correlations Zhou et al. (2018)
    Network across diferent systems
    Spatially resolved network
    Bacteria Seawater Water depth Extended local similarity analysis Cram et al. (2015)
    Bacteria Seawater Particle size SparCC Milici et al. (2016)
    Bacteria and archaea Estuary Water and sediment Spearman's rank correlations Wei et al. (2016)
    Bacteria Seawater Water depth Spearman's rank correlations Cui et al. (2019)
    Temporally resolved network
    Bacteria and archaea Seawater (deep chlorophyll maximum) Month Local similarity analysis Beman et al. (2011)
    Bacteria Seawater Month Extended local similarity analysis Cram et al. (2015)
    Bacteria, myoviruses and phytoplankton Seawater Daily to weekly Local similarity analysis Needham et al. (2017)
    Protist Seawater Daily to weekly Extended local similarity analysis Berdjeb et al. (2018)
    Bacteria and archaea Seawater Season SparCC Chafee et al. (2018)
     | Show Table
    DownLoad: CSV

    Several studies have attempted to use networks to infer potential functional couplings between microbes. For example, Thaumarchaeota Marine Group I (MG-I), the most abundant archaeal clade in the marine environment, capable of ammonia oxidization, has been found to co-occur with Nitrospina (Reji et al. 2019) and/or with Nitrospira when Nitrospina is absent or in low abundance (Wang et al. 2019), both of which are nitrite oxidizers. Their co-occurrence in seawater is supported by substrate feeding (nitrite produced by MG-I is the substrate of Nitrospina/Nitrospira) and facilitates the complete nitrifcation process. Previous eforts to explore co-occurrence patterns between functional bacteria in marine sediments have demonstrated signifcant correlations between sulfate-reducing bacteria and sulfuroxidizing bacteria, and between sulfate-reducing bacteria and nitrite-oxidizing bacteria (Liu et al. 2014b). Elucidation of co-occurrence patterns with functional gene abundance derived from GeoChip and metagenome may facilitate a more direct inference. However, the obtained co-occurrence patterns should be treated with caution when used to infer functional couplings, since they are not necessarily refecting real interactions.

    Classically, a network describes co-occurrence patterns between taxa. However, environmental variables can also be included to explore microbe-environment relationships. Additionally, considering the natural complexity of inter taxa relationships in an ecosystem, pairwise microbe-microbe correlations, derived from most current network analyses, need to be expanded to a higher order, such as three- or fourway correlations. The high-order microbial co-occurrence patterns may involve possible disruption or enhancement of another taxon to a pairwise relationship (Bairey et al. 2016). Such high-order co-occurrence patterns can also be unraveled by analyzing compositional data, as long as new and proper statistical tools are developed (Bairey et al. 2016). Although co-occurrence patterns are not appropriate to imply accurate microbial interactions, their spatiotemporal dynamics hold the potential to afect the assembling processes and ecological roles of microbial communities.

    To better understand microbial ecosystem functioning, creating links between an individual taxon and a specifc function is required. However, it is infeasible to trace all the diverse biogeochemical processes and to relate them to taxa. This problem may be solved from the point of view of the microorganisms, as microbial functional capabilities have been found to connect strongly with phylogeny (Martiny et al. 2013; Zimmerman et al. 2013). For example, the presence of functional genes related to oxygenic photosynthesis, methane oxidation and sulfate reduction has been found to be highly phylogenetically conserved (Martiny et al. 2013). In coastal seawater, recent studies have shown that microorganisms that assimilated organic matter, including starch and glucose, were phylogenetically clustered (Bryson et al. 2017; Mayali and Weber 2018), refecting phylogenetically conserved resource partitioning in the coastal microbial loop (Bryson et al. 2017). Such phylogenetic conservation in substrate utilization supports similar distribution patterns (even at a broader taxonomic level; Philippot et al. 2010; Schmidt et al. 2016) and similar lifestyles among microbial relatives. Salazar et al. (2015) found that the particle-associated and free-living populations in the deep ocean had diferent phylogenetic origins. These observations enhance the possibility of inferring microbial functional traits with phylogenetic information.

    However, growing evidence now suggests that variations in functional traits occur within closely related microbes, even at the loosely defned species level (Larkin and Martiny 2017). Prochlorococcus, the most abundant genus of photosynthetic organisms, diverges into high- and low-lightadapted ecotypes, which display diferent light-harvesting strategies (Bibby et al. 2003). Likewise, Alteromonas macleodii, a typical copiotrophic r-strategist, contains both surface and deep-sea ecotypes (Ivars-Martinez et al. 2008), which have been shown to difer substantially in their capacity to degrade algal polysaccharides (Neumann et al. 2015). On the other hand, microorganisms performing similar metabolic functions can be only distantly related (Martiny et al. 2015), the basic principle of functional redundancy. Louca et al.(2016, 2017) found high functional redundancy in both marine and plant-associated microbial communities, implying that microbial functional traits are widely spread among microbial lineages.

    Horizontal gene transfer and gene gain and loss likely result in the discrepancy in phylogeny-functional trait relationships (Fig. 2a). The type of functional trait is also an important contributor, with traits with slower evolutionary rates displaying clearer phylogenetically conserved patterns. Bryson et al. (2017) reported that traits of resource utilization in marine microbes, represented by patterns of substrate assimilation, were phylogenetically cohesive, whereas those of biosynthetic activity after assimilation were heterogeneous. Additionally, functional potential (gene presence) does not necessarily mean function execution (gene expression) and functional capability is not equal to rate (the same functional trait can be diferent in rate). Although the capability of glucose incorporation is widespread in bacteria and displays a shallow phylogenetic clustering (Martiny et al. 2013), the glucose assimilation rates in soil bacteria have been observed to vary greatly across phylogeny and display a deep phylogenetic clustering (Morrissey et al. 2016). This fnding highlights the importance of incorporating functional rates into phylogeny-function relatedness and raises the need to examine how quantitative changes in microbial function afect ecosystem functioning.

    Figure  2.  Relationships among microbial phylogeny, diversity and ecosystem functioning: (a) the relationship between phylogeny and function is complex, although many functional traits are phylogenetically conserved. Possible reasons for the decoupling of phylogeny and function are presented; (b) microbial diversity (species richness, functional and phylogenetic diversity) is increasingly shown to be positively correlated to ecosystem functioning, whereas negative correlations are also observed. These correlations stimulate a great interest in predicting ecosystem functioning with microbial data. Inclusion of both environmental and microbial data (including microbial interactions and omic data) will enhance the power of ecosystem functioning prediction

    There is growing evidence of a positive relationship between microbial diversity and ecosystem functioning (Cardinale et al. 2012; Delgado-Baquerizo et al. 2016b; Schnyder et al. 2018), although negative or no relationships have also been reported (Becker et al. 2012). Such relationships are derived primarily from studies on the terrestrial environment and have rarely been assessed for marine microbial communities. A study of microbial diversity-ecosystem functioning (DEF) relationship in marine surface water also supported a positive correlation, showing that a more phylogenetically diverse bacterial community had a greater level of ecosystem functioning (heterotrophic productivity measured by leucine incorporation; Galand et al. 2015). The enhancement of ecosystem functioning by increased biodiversity is thought to result from complementarity (minimal overlap) in resource use by functionally distinct taxa (Petchey and Gaston 2002) and/or through inter taxa facilitation (Hooper et al. 2005). Therefore, the relationship between diversity and ecosystem functioning is controlled by the niche-based mechanisms: diferentiation in resource niche and selection efect (Krause et al. 2014).

    The few studies that investigated the shape of the positive relationship between microbial diversity and ecosystem functioning have frequently uncovered a more linear relationship (Delgado-Baquerizo et al. 2016a) than the approaching-fat relationship seen for plants and animals (Cardinale et al. 2011). Such a linear relationship implies an indefnite increase of ecosystem functioning with increasing microbial diversity, challenging the idea of functional redundancy as mentioned above. In fact, Galand et al. (2018) provide evidence against the hypothesis of functional redundancy by showing a strong link between marine microbial community compositions and functional attributes using all the set of metagenomic reads. The authors emphasize the need to consider all functional aspects rather than relying only on known genes in investigating microbial DEF relationships. In addition, diferent processing rates seen in the same functional trait (Morrissey et al. 2016) may also provide opposing evidence against functional redundancy. However, these fndings do not rule out the possibility for a partial functional redundancy, implicating that diferent types of functional traits may have diferent levels of redundancy. The idea of functional redundancy on the one hand can help to explain the high level of marine microbial diversity (diferent taxa are supported by a limited range of resources and conduct the same set of metabolic processes; Allison and Martiny 2008), while on the other hand can limit the extent of ecosystem functioning.

    Diversity is composed of diferent components, including richness (taxonomic diversity), phylogeny (phylogenetic diversity) and function (functional diversity) (Fig. 2b). Diferent types of diversity can inform distinct microbial DEF relationships. However, taxonomic diversity is the more frequently used proxy in inferring DEF relationships, compared to functional diversity and phylogenetic diversity. It has been reported that taxonomic diversity has relatively little impact on ecosystem functioning (Nielsen et al. 2011), while functional diversity was more correlated, mostly likely by determining ecological niches and inter taxa interactions (Hooper et al. 2005; Krause et al. 2014). Nevertheless, functional diversity is always difcult to measure (functional activity) and/or requires additional sequencing eforts to analyze (functional genes). Thus, phylogenetic diversity is increasingly implemented as a proxy of functional diversity, with the thought that many functional traits are phylogenetically conserved. Indeed, a positive correlation has been found between marine surface bacterial productivity and phylogenetic diversity of the active community; no similar association was found when taxonomic diversity (Shannon index) was analyzed (Galand et al. 2015). The fndings of Galand et al. (2015) highlighted that ecosystem functioning is related to the active rather than the total community that contains dormant taxa. This provides an explanation for the more frequently observed negative and/or no relationships between phylogenetic diversity of the total community and ecosystem functioning (Goberna and Verdu 2018; Pérez-Valera et al. 2015; Severin et al. 2013). The relationship between phylogenetic diversity and ecosystem functioning also relates to taxon-specifc functional capability and evolutionary history (Gravel et al. 2012). Under which conditions phylogenetic diversity can be used as a representative of functional diversity should be characterized further.

    The microbial DEF relationship can be confounded by environmental variations, as environmental factors can exert infuences on both diversity and ecosystem functioning. Orland et al. (2018) demonstrated that pH and organic matter quantity and quality explained as much variation in CO2 production as did taxonomic diversity in lake sediments; these environmental factors exerted direct infuences on ecosystem functioning due to their unrelatedness to taxonomic diversity. Comparatively, Delgado-Baquerizo et al. (2016b) found in a global set of soil samples that the DEF relationship was maintained when accounting for edaphic factors, which suggests that taxonomic diversity can exert infuences on ecosystem functioning independently of environmental variabilities. A global survey of microbiome in seawater showed a decoupling of taxonomy and function, with the latter being more susceptible to environmental changes (Louca et al. 2016). Environmental conditions determine the availability of electronic donors/acceptors to microbes and shape the process of biogeochemical reactions. In addition to the environment, stochastic processes may also afect diversity and infuence ecosystem functioning (Orland et al. 2018; Zhou et al. 2013). Overall, the positive DEF relationship in microorganisms is supportive of phylogenetic conservation in functional traits. More efort is needed to discern the role of diferent diversity components and the role of deterministic and stochastic processes in determining ecosystem functioning.

    The abovementioned relationships have stimulated great interest in using microbial data to predict ecosystem functioning (statistical simulation instead of direct measurement) (Graham et al. 2016; Powell et al. 2015b) (Fig. 2b). Here, we focus on the interactions between community (diversity and abundance) and ecosystem functioning, although physiological properties can also be related (Wieder et al. 2013). Graham et al. (2016) synthesized 82 global datasets from diferent ecosystems to improve the predictive power of carbon and nitrogen processing rates by the inclusion of the microbial community data. They found that the addition of both compositional and diversity data could strengthen the predictive power, although this was not applicable to all datasets. Andersson et al. (2014) demonstrated, via structural equation models, that the model that included total bacterial abundance explained 54% of the variation in nitrogenase activity in coastal sediments and by replacing total bacterial abundance with cyanobacterial biomass it could increase the predictive power.

    The explanatory power of microbial data in predictive models is always lower than that of abiotic factors (Graham et al. 2014, 2016; Powell et al. 2015b), consistent with the notion that environmental factors have direct impacts on ecosystem functioning. Moreover, under diferent environmental conditions (e.g., temperature, Dolan et al. 2017), the explanatory power of microbial data may change. However, this does not decrease the importance of microbial data in functional prediction. Recently, Zhang et al. (2018) found that in coastal sediments adding diferent copy number ratios of functional and rRNA genes into stepwise regression models substantially increased the predictive power of denitrifcation and anammox rates, although alpha diversity and gene abundance of involved bacteria were poorly correlated to the function potentials. In addition to abundance and diversity, it is also important to include microbial interactions to the predictive model in future studies (Fig. 2b). In summary, knowledge on the distribution patterns of microbial communities is indispensable for understanding their biogeochemical and ecological functions.

    As stated above, a microbial community contains both active and dormant members. Dormant microbes constitute the seed bank of a community. Their repeated entrance to and exit from the seed bank decouple the active and total fractions (Jones and Lennon 2010; Fig. 3). Since RNA is a good indicator of whether or not a microbe is viable, rRNA based methods have been extensively used to characterize the active community, despite the difculty in RNA extraction and the probable biases introduced by reverse transcription.

    Figure  3.  Environmental shifts will change the relative abundance of the dormant and active fractions within a microbial community. Such changes will cause shifts in microbial co-occurrence patterns and fnally afect ecosystem functioning

    Mounting evidence suggests that there is a signifcant diference between the total (resident) and active fractions within a microbial community. Several abundant taxa are less active in the RNA pool, whereas some highly active taxa show low abundance or are almost absent in the DNA pool (Baldrian et al. 2012; Richa et al. 2017; Romanowicz et al. 2016; Sebastián et al. 2018). For example, Cyanobacteria and the SAR11 clade of Alphaproteobacteria are the most abundant microbes in the global surface ocean; whereas the former is always disproportionately active (16S rRNA:rDNA > 1), the latter tends to be less active (Campbell and Kirchman 2013; Hunt et al. 2013; Zhang et al. 2014). Further, a refned phylogenetic analysis showed that diferent ecotypes of the SAR11 clade varied in their 16S rRNA:rDNA ratios (Salter et al. 2015). A similar phenomenon was also shown for diferent ecotypes of MG-I (Hugoni et al. 2013). Within a microbial community, activity can also vary between rare and abundant taxa (Campbell et al. 2011; Richa et al. 2017). Richa et al. (2017) reported that more than 70% of the rare taxa in coastal seawater of the Mediterranean Sea had high 16S rRNA:rDNA ratios. To explain this decoupling of abundance and activity, Campbell et al. (2011) proposed that a substantial proportion of bacteria became active when their abundance decreased, indicating that high abundance may be a constraint factor for activity or that top-down processes i.e., grazing and virus lysis could stimulate activity. Seasonality (Hugoni et al. 2013), environmental factors, such as salinity (Campbell and Kirchman 2013), and lifestyle modes (free-living and particle-attached; Li et al. 2018) have also been reported as drivers for 16S rRNA:rDNA ratio variations.

    The active and total microbial communities have been found to display contrasting biogeographic patterns and respond diferently to environmental factors in seawater (Zhang et al. 2014). Environmental changes would generate uncomfortable conditions for active microbes, and the adaptation and successful establishment of active microbes in a new environment are difcult (Hanson et al. 2012). By contrast, the growth of several dormant microbes can be stimulated by changing environments, contributing to microbial community succession. Considering this, the active community is likely to display a stronger distance-decay relationship than the total community (Zhang et al. 2014). Nevertheless, our understanding of the assembling processes (relative role of deterministic and stochastic processes) of the total and active communities is limited. Zhang et al. (2014) also found that the active (dominated by negative correlations) and total (dominated by positive correlations) bacterial communities exhibited diferent co-occurrence patterns. Frequent transitions of microbes between an active or dormant status under changing environments would lead to variations in co-occurrence patterns, causing signifcant alterations in ecosystem functioning (Fig. 3). As mentioned above, active microbes are directly linked to ecosystem functioning by actively carrying out biogeochemical reactions (Nannipieri et al. 2003). Thus, distinguishing the active fraction from the whole community would provide novel insights into patterns of microbial assembly, co-occurrence and DEF relationship. Moreover, the fnding of a higher environmental sensitivity of active heterotrophs than active autotrophs in seawater (Zhang et al. 2014) further raises the need to treat functionally diferent microbial groups separately.

    Another possible utilization of the rRNA:rDNA ratio is to indicate potential growth rate (Campbell et al. 2011; Lankiewicz et al. 2016), as numerous microorganisms are yet to be cultivated and their growth rates are not able to be measured (Kirchman 2016). A high rRNA:rDNA ratio may imply a high growth rate. Thus, the lower proportion of SAR11 in the RNA than in the DNA pool, as mentioned above, may indicate a slow growth mode, although it may also be due to the low number of ribosomes per cell, given its small cell size. The slow growth rate of SAR11, however, is further verifed by culture-based analyses (Lankiewicz et al. 2016). In comparison, copiotrophic taxa from Alteromonas and the Rosebacter clade often display higher growth rates (Hunt et al. 2013; Lankiewicz et al. 2016). Noticeably, the rRNA:rDNA ratio has been reported to be not always efective in quantifying microbial growth rates, and protein synthesis potential has been proposed to be a more suitable interpretation (Blazewicz et al. 2013).

    The ribosomal gene sequences obtained from the marine environments using culture-independent methods have signifcantly expanded the microbial phylogenetic tree and public rRNA gene databases (the most popular are SILVA, Greengenes and RDP databases) (Brown et al. 2015; Delong 1992; Hug et al. 2016; Kubo et al. 2012). The microbial groups that have no close isolates at the time of discovering their rRNA gene sequences are often indicated by informal nomenclature, such as SAR11, MG-I and Miscellaneous Crenarchaeota Group (MCG). Further, in-depth phylogenetic analyses of the rRNA gene sequences have clustered many microbial groups, such as MG-I and MCG, into subclades (Kubo et al. 2012; Liu et al. 2014a). These subclades have been shown to respond diferently to environmental changes and exhibit diferent habitat preferences (Lazar et al. 2016; Liu et al. 2014a). Similar niche diferentiations are also shown for marine bacteria sharing high 16S rRNA gene similarities (e.g., Alteromonas macleodii as mentioned above). These observations suggest that environmental selection plays a crucial role in the process of microbial evolution. In addition to rRNA genes, functional genes can be used to investigate the diversifcation of functional groups. For example, Alves et al. (2018) recently elucidated the global frequency, phylogenetic diversity and habitat specifcity of ammonia-oxidizing archaea using amoA, the gene encoding the active-site subunit of ammonia monooxygenase. These results highlight the importance of using community data derived from molecular marker genes to investigate the phylogenetic relationships and to infer the evolutionary histories of diferent microbial taxa.

    However, a single marker gene is not always efective in diferentiating phylogenetically close relatives. In this context, the multilocus sequence typing (MLST) analysis, which takes the phylogenetic information of several (usually 5–7) housekeeping genes, has been shown to provide a better resolution (Enright and Spratt 1999). In recent years, the increasing number of public metagenomic/genomic sequences has provided an excellent resource for determining phylogenetic relatedness among microbes with a high confdence level (Brown et al. 2015; Hug et al. 2016). These phylogenomic analyses have enabled the designation of many novel microbial phyla, including the well-known Thaumarchaeota (containing MG-I) and Bathyarchaeota (MCG) (Adam et al. 2017). Spang et al. (2015) proposed a new archaeal phylum Lokiarchaeota through phylogenomic inference. This phylum contains many eukaryotic signatures, signifcantly contributing to our understanding of the evolution of life.

    The prevalence of studies on microbial communities in the marine environment benefts from the development of new sequencing technologies. The resulting increase in sequencing depth facilities the obtaining of accurate insights into microbial community structure, and in particular enhances the capability of distinguishing rare subcommunities from sequencing errors. In the era of big data, the development of sequencing technologies calls for a simultaneous introduction of new statistical methods and tools, which would help to discern microbial assembling processes and unravel highorder (three- or four-way) microbe-microbe interactions that most likely occur in natural environments. Although microbe-microbe interactions, to date derived mainly from co-occurrence networks, are important in structuring microbial communities and mediating ecological functions, such linkages are still largely elusive. Suitable analytic tools are required to construct a model that bridges the gap between microbial interactions and ecosystem functioning.

    Owing to the difculty in measuring microbial functions, inclusion of community data in the predictive modeling of ecosystem functioning is receiving increasing attention. This raises associated questions such as whether diferent functional types exhibit similar sensitivity to community data and vice versa, and whether relationships between community data and ecosystem functioning vary spatially and temporally. In addition, the decoupling of phylogeny and function may act as an obstacle for such modeling, which calls for a resolved phylogenetic clustering and taxon-specifc functional characterization. Omics, such as metagenome, single-cell genome and metatranscriptome, in parallel with advanced analytic tools, provide great opportunities to link a community, and further to link an individual to function (Fig. 2b).

    In this review, we highlight the signifcance of separating a whole microbial community into subgroups according to diferent standards. The abundance-dependent grouping has led to the realization that rare subcommunities, the members of which often show high activity, have the potential to increase the power of ecosystem functioning prediction. By contrast, functional-, and other traits-dependent grouping have received less attention. After it has been established what exists, it is then necessary to determine what is alive and whether the active taxa follow patterns seen for the total community, and how active taxa contribute to ecosystem functioning. We also need to know if functional traits of the active community are phylogenetically organized, because such information is important for constructing a direct linkage between community and ecosystem functioning. In summary, subdivision of the whole community will provide accurate and novel insights into relationships between microbial diversity, interaction and ecosystem functioning.

    Acknowledgements This work was supported by the National Natural Science Foundation of China (Grants Nos. 41976101, 41506154 and 41730530) and the Fundamental Research Funds for the Central Universities (Grants No. 201762017).

    Author's Contribution XZ conceived, provided the idea to this work and edited the manuscript; JL, ZM and XL wrote the manuscript; JL prepared the fgures and tables. All authors approved the fnal manuscript.

    The authors declare that they have no confict of interest.

    This article does not contain any studies with human participants or animals performed by any of the authors.

    This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativeco mmons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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