Fungi contribute extensively to a wide range of ecosystem processes, including decomposition of organic carbon, deposition of recalcitrant carbon, and transformations of nitrogen and phosphorus. In ...this review, we discuss the current knowledge about physiological and morphological traits of fungi that directly influence these processes, and we describe the functional genes that encode these traits. In addition, we synthesize information from 157 whole fungal genomes in order to determine relationships among selected functional genes within fungal taxa. Ecosystem-related traits varied most at relatively coarse taxonomic levels. For example, we found that the maximum amount of variance for traits associated with carbon mineralization, nitrogen and phosphorus cycling, and stress tolerance could be explained at the levels of order to phylum. Moreover, suites of traits tended to co-occur within taxa. Specifically, the genetic capacities for traits that improve stress tolerance-β-glucan synthesis, trehalose production, and cold-induced RNA helicases-were positively related to one another, and they were more evident in yeasts. Traits that regulate the decomposition of complex organic matter-lignin peroxidases, cellobiohydrolases, and crystalline cellulases-were also positively related, but they were more strongly associated with free-living filamentous fungi. Altogether, these relationships provide evidence for two functional groups: stress tolerators, which may contribute to soil carbon accumulation via the production of recalcitrant compounds; and decomposers, which may reduce soil carbon stocks. It is possible that ecosystem functions, such as soil carbon storage, may be mediated by shifts in the fungal community between stress tolerators and decomposers in response to environmental changes, such as drought and warming.
Dormancy is a bet-hedging strategy used by a wide range of taxa, including microorganisms. It refers to an organism's ability to enter a reversible state of low metabolic activity when faced with ...unfavourable environmental conditions. Dormant microorganisms generate a seed bank, which comprises individuals that are capable of being resuscitated following environmental change. In this Review, we highlight mechanisms that have evolved in microorganisms to allow them to successfully enter and exit a dormant state, and discuss the implications of microbial seed banks for evolutionary dynamics, population persistence, maintenance of biodiversity, and the stability of ecosystem processes.
Global change is challenging plant and animal populations with novel environmental conditions, including increased atmospheric CO ₂ concentrations, warmer temperatures, and altered precipitation ...regimes. In some cases, contemporary or “rapid” evolution can ameliorate the effects of global change. However, the direction and magnitude of evolutionary responses may be contingent upon interactions with other community members that also are experiencing novel environmental conditions. Here, we examine plant adaptation to drought stress in a multigeneration experiment that manipulated aboveground–belowground feedbacks between plants and soil microbial communities. Although drought stress reduced plant growth and accelerated plant phenologies, surprisingly, plant evolutionary responses to drought were relatively weak. In contrast, plant fitness in both drought and nondrought environments was linked strongly to the rapid responses of soil microbial community structure to moisture manipulations. Specifically, plants were most fit when their contemporary environmental conditions (wet vs. dry soil) matched the historical environmental conditions (wet vs. dry soil) of their associated microbial community. Together, our findings suggest that, when faced with environmental change, plants may not be limited to “adapt or migrate” strategies; instead, they also may benefit from association with interacting species, especially diverse soil microbial communities, that respond rapidly to environmental change.
In ecology, biodiversity-ecosystem functioning (BEF) research has seen a shift in perspective from taxonomy to function in the last two decades, with successful application of trait-based approaches. ...This shift offers opportunities for a deeper mechanistic understanding of the role of biodiversity in maintaining multiple ecosystem processes and services. In this paper, we highlight studies that have focused on BEF of microbial communities with an emphasis on integrating trait-based approaches to microbial ecology. In doing so, we explore some of the inherent challenges and opportunities of understanding BEF using microbial systems. For example, microbial biologists characterize communities using gene phylogenies that are often unable to resolve functional traits. Additionally, experimental designs of existing microbial BEF studies are often inadequate to unravel BEF relationships. We argue that combining eco-physiological studies with contemporary molecular tools in a trait-based framework can reinforce our ability to link microbial diversity to ecosystem processes. We conclude that such trait-based approaches are a promising framework to increase the understanding of microbial BEF relationships and thus generating systematic principles in microbial ecology and more generally ecology.
Dormancy is a bet-hedging strategy used by a variety of organisms to overcome unfavorable environmental conditions. By entering a reversible state of low metabolic activity, dormant individuals ...become members of a seed bank, which can determine community dynamics in future generations. Although microbiologists have documented dormancy in both clinical and natural settings, the importance of seed banks for the diversity and functioning of microbial communities remains untested. Here, we develop a theoretical model demonstrating that microbial communities are structured by environmental cues that trigger dormancy. A molecular survey of lake ecosystems revealed that dormancy plays a more important role in shaping bacterial communities than eukaryotic microbial communities. The proportion of dormant bacteria was relatively low in productive ecosystems but accounted for up to 40% of taxon richness in nutrient-poor systems. Our simulations and empirical data suggest that regional environmental cues and dormancy synchronize the composition of active communities across the landscape while decoupling active microbes from the total community at local scales. Furthermore, we observed that rare bacterial taxa were disproportionately active relative to common bacterial taxa, suggesting that microbial rank-abundance curves are more dynamic than previously considered. We propose that repeated transitions to and from the seed bank may help maintain the high levels of microbial biodiversity that are observed in nearly all ecosystems.
Microbiomes in light of traits: A phylogenetic perspective Martiny, Jennifer B. H.; Jones, Stuart E.; Lennon, Jay T. ...
Science (American Association for the Advancement of Science),
11/2015, Volume:
350, Issue:
6261
Journal Article
Peer reviewed
Open access
A focus on the phenotypic characteristics of microorganisms-their traits-offers a path for interpreting the growing amount of microbiome data. We review key aspects of microbial traits, as well as ...approaches used to assay their phylogenetic distribution. Recent studies reveal that microbial traits are differentially conserved across the tree of life and appear to be conserved in a hierarchical fashion, possibly linked to their biochemical complexity. These results suggest a predictive framework whereby the genetic (or taxonomic) resolution of microbiome variation among samples provides information about the traits under selection. The organizational parallels seen among human and free-living microbiomes seem to support this idea. Developments in this framework may offer predictions not only for how microbial composition responds to changing environmental conditions, but also for how these changes may alter the health or functioning in human, engineered, and environmental systems.
Microorganisms play a central role in the regulation of ecosystem processes, and they comprise the vast majority of species on Earth. With recent developments in molecular methods, it has become ...tractable to quantify the extent of microbial diversity in natural environments. Here we examine this revolution in our understanding of microbial diversity, and we explore the factors that contribute to the seemingly astounding numbers of microbial taxa found within individual environmental samples. We conducted a meta-analysis of bacterial richness estimates from a variety of ecosystems. Nearly all environments contained hundreds to thousands of bacterial taxa, and richness levels increased with the number of individuals in a sample, a pattern consistent with those reported for nonmicrobial taxa. A cursory comparison might suggest that bacterial richness far exceeds the richness levels typically observed for plant and animal taxa. However, the apparent diversity of bacterial communities is influenced by phylogenetic breadth and allometric scaling issues. When these features are taken into consideration, the levels of microbial diversity may appear less astounding. Although the fields of ecology and biogeography have traditionally ignored microorganisms, there are no longer valid excuses for neglecting microorganisms in surveys of biodiversity. Many of the concepts developed to explain plant and animal diversity patterns can also be applied to microorganisms once we reconcile the scale of our analyses to the scale of the organisms being observed. Furthermore, knowledge from microbial systems may provide insight into the mechanisms that generate and maintain species richness in nonmicrobial systems.
Abstract
Microbes regulate the composition and turnover of organic matter. Here we developed a framework called Energy-Diversity-Trait integrative Analysis to quantify how dissolved organic matter ...and microbes interact along global change drivers of temperature and nutrient enrichment. Negative and positive interactions suggest decomposition and production processes of organic matter, respectively. We applied this framework to manipulative field experiments on mountainsides in subarctic and subtropical climates. In both climates, negative interactions of bipartite networks were more specialized than positive interactions, showing fewer interactions between chemical molecules and bacterial taxa. Nutrient enrichment promoted specialization of positive interactions, but decreased specialization of negative interactions, indicating that organic matter was more vulnerable to decomposition by a greater range of bacteria, particularly at warmer temperatures in the subtropical climate. These two global change drivers influenced specialization of negative interactions most strongly via molecular traits, while molecular traits and bacterial diversity similarly affected specialization of positive interactions.
Dormancy is a life history trait that may have important implications for linking microbial communities to the functioning of natural and managed ecosystems. Rapid changes in environmental cues may ...resuscitate dormant bacteria and create pulses of ecosystem activity. In this study, we used heavy-water (H(18) 2O) stable isotope probing (SIP) to identify fast-growing bacteria that were associated with pulses of trace gasses (CO2, CH4, and N2O) from different ecosystems agricultural site, grassland, deciduous forest, and coniferous forest (CF) following a soil-rewetting event. Irrespective of ecosystem type, a large fraction (69-74%) of the bacteria that responded to rewetting were below detection limits in the dry soils. Based on the recovery of sequences, in just a few days, hundreds of rare taxa increased in abundance and in some cases became dominant members of the rewetted communities, especially bacteria belonging to the Sphingomonadaceae, Comamonadaceae, and Oxalobacteraceae. Resuscitation led to dynamic shifts in the rank abundance of taxa that caused previously rare bacteria to comprise nearly 60% of the sequences that were recovered in rewetted communities. This rapid turnover of the bacterial community corresponded with a 5-20-fold increase in the net production of CO2 and up to a 150% reduction in the net production of CH4 from rewetted soils. Results from our study demonstrate that the rare biosphere may account for a large and dynamic fraction of a community that is important for the maintenance of bacterial biodiversity. Moreover, our findings suggest that the resuscitation of rare taxa from seed banks contribute to ecosystem functioning.
The biodiversity of microbial communities has important implications for the stability and functioning of ecosystem processes. Yet, very little is known about the environmental factors that define ...the microbial niche and how this influences the composition and activity of microbial communities. In this study, we derived niche parameters from physiological response curves that quantified microbial respiration for a diverse collection of soil bacteria and fungi along a soil moisture gradient. On average, soil microorganisms had relatively dry optima (0.3 MPa) and were capable of respiring under low water potentials (−2.0 MPa). Within their limits of activity, microorganisms exhibited a wide range of responses, suggesting that some taxa may be able to coexist by partitioning the moisture niche axis. For example, we identified dry-adapted generalists that tolerated a broad range of water potentials, along with wet-adapted specialists with metabolism restricted to less-negative water potentials. These contrasting ecological strategies had a phylogenetic signal at a coarse taxonomic level (phylum), suggesting that the moisture niche of soil microorganisms is highly conserved. In addition, variation in microbial responses along the moisture gradient was linked to the distribution of several functional traits. In particular, strains that were capable of producing biofilms had drier moisture optima and wider niche breadths. However, biofilm production appeared to come at a cost that was reflected in a prolonged lag time prior to exponential growth, suggesting that there is a trade-off associated with traits that allow microorganisms to contend with moisture stress. Together, we have identified functional groups of microorganisms that will help predict the structure and functioning of microbial communities under contrasting soil moisture regimes.
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