Winter is recognized as an important time for microbial activity that influences biogeochemical cycles. The onset of the winter snowpack in temperate hardwood ecosystems has been and will continue to ...be delayed over the next century. The decline in snowpack results in more soil freeze–thaw events and lower winter soil temperatures. Understanding microbial responses to varying snowpack conditions is important to understanding the effect of climate change on forest ecosystems. To this end, we removed snow to simulate a thinner, more ephemeral snowpack at two sites in the northeastern US, Harvard Forest (MA) and Hubbard Brook Experimental Forest (NH). We then measured microbial and exoenzyme activity in soils following snowmelt and three additional time points across the growing season. We found that microbial and exoenzyme activity were both positively correlated with the depth and duration of the snowpack at each site. The depth and duration of soil frost were negatively correlated with microbial biomass, exoenzyme activity and respiration, but only at Harvard Forest and not at Hubbard Brook. At both sites the changes in microbial and exoenzyme activity were transient and did not persist into the growing season past tree leaf-out. While it is possible that reductions in the snowpack and changes to microbial activity in the early spring may lead to asynchrony in the phenology of microbial relative to plant activity, it is at present uncertain whether and over what time scale this asynchrony may affect other forest ecosystem processes.
Winter air temperatures are rising faster than summer air temperatures in high-latitude forests, increasing the frequency of soil freeze/thaw events in winter. To determine how climate warming and ...soil freeze/thaw cycles affect soil microbial communities and the ecosystem processes they drive, we leveraged the Climate Change across Seasons Experiment (CCASE) at the Hubbard Brook Experimental Forest in the northeastern United States, where replicate field plots receive one of three climate treatments: warming (+5°C above ambient in the growing season), warming in the growing season + winter freeze/thaw cycles (+5°C above ambient +4 freeze/thaw cycles during winter), and no treatment. Soil samples were taken from plots at six time points throughout the growing season and subjected to amplicon (rDNA) and metagenome sequencing. We found that soil fungal and bacterial community composition were affected by changes in soil temperature, where the taxonomic composition of microbial communities shifted more with the combination of growing-season warming and increased frequency of soil freeze/thaw cycles in winter than with warming alone. Warming increased the relative abundance of brown rot fungi and plant pathogens but decreased that of arbuscular mycorrhizal fungi, all of which recovered under combined growing-season warming and soil freeze/thaw cycles in winter. The abundance of animal parasites increased significantly under combined warming and freeze/thaw cycles. We also found that warming and soil freeze/thaw cycles suppressed bacterial taxa with the genetic potential for carbon (i.e., cellulose) decomposition and soil nitrogen cycling, such as N fixation and the final steps of denitrification. These new soil communities had higher genetic capacity for stress tolerance and lower genetic capacity to grow or reproduce, relative to the communities exposed to warming in the growing season alone. Our observations suggest that initial suppression of biogeochemical cycling with year-round climate change may be linked to the emergence of taxa that trade-off growth for stress tolerance traits.
Microorganisms of the soil‐root continuum play key roles in ecosystem function. The Loess Plateau is well known for its severe soil erosion and thick loess worldwide, where mean annual precipitation ...(MAP) and soil nutrients decrease from the southeast to the northwest. However, the relative influence of environmental factors on the microbial community in four microhabitats (bulk soil, rhizosphere, rhizoplane, and endosphere) in the soil‐root continuum along the environmental gradient in the Loess Plateau remains unclear. In this study, we investigated 82 field sites from warm‐temperate to desert grasslands across the Loess Plateau, China, to assess the bacterial diversity, composition, community assembly, and co‐occurrence networks in the soil‐root continuum along an environmental gradient using bacterial 16S recombinant DNA amplicon sequencing. We discovered that the microhabitats explained the largest source of variations in the bacterial diversity and community composition in this region. Environmental factors (e.g., MAP, soil organic carbon, and pH) impacted the soil, rhizosphere, and rhizoplane bacterial communities, but their effects on the bacterial community decreased with increased proximity to roots from the soil to the rhizoplane, and the MAP enlarged the dissimilarity of microbial communities from the rhizosphere and rhizoplane to bulk soil. Additionally, stochastic assembly processes drove the endosphere communities, whereas the soil, rhizosphere, and rhizoplane communities were governed primarily by the variable selection of deterministic processes, which showed increased importance from warm‐temperate to desert grasslands. Moreover, the properties of the microbial networks in the rhizoplane community indicate more stable networks in desert grasslands, likely conferring the resistance of microbial communities in higher stress environments. Collectively, our results showed that the bacterial communities in the soil‐root continuum had different sensitivities and assembly mechanisms along an environmental gradient. These patterns are shaped simultaneously by the intertwined dimensions of proximity to roots and environmental stress change in the Loess Plateau.
Changes in microbes in the soil‐root continuum along an environmental gradient were investigated. The soil, rhizosphere and rhizoplane communities were governed by deterministic processes. Environmental stress enlarged the dissimilarity of microbial communities in the soil‐root continuum. Root‐associated microbiomes did not destabilize at locations with higher environmental stress.
Highlights
Changes in microbes in the soil‐root continuum along an environmental gradient were investigated.
The soil, rhizosphere and rhizoplane communities were governed by deterministic processes.
Environmental stress enlarged the dissimilarity of microbial communities in the soil‐root continuum.
Root‐associated microbiomes did not destabilize at locations with higher environmental stress.
Climate models project an increase in mean annual air temperatures and a reduction in the depth and duration of winter snowpack for many mid and high latitude and high elevation seasonally ...snow-covered ecosystems over the next century. The combined effects of these changes in climate will lead to warmer soils in the growing season and increased frequency of soil freeze-thaw cycles (FTCs) in winter due to the loss of a continuous, insulating snowpack. Previous experiments have warmed soils or removed snow via shoveling or with shelters to mimic projected declines in the winter snowpack. To our knowledge, no experiment has examined the interactive effects of declining snowpack and increased frequency of soil FTCs, combined with soil warming in the snow-free season on terrestrial ecosystems. In addition, none have mimicked directly the projected increase in soil FTC frequency in tall statured forests that is expected as a result of a loss of insulating snow in winter. We established the Climate Change Across Seasons Experiment (CCASE) at Hubbard Brook Experimental Forest in the White Mountains of New Hampshire in 2012 to assess the combined effects of these changes in climate on a variety of pedoclimate conditions, biogeochemical processes, and ecology of northern hardwood forests. This paper demonstrates the feasibility of creating soil FTC events in a tall statured ecosystem in winter to simulate the projected increase in soil FTC frequency over the next century and combines this projected change in winter climate with ecosystem warming throughout the snow-free season. Together, this experiment provides a new and more comprehensive approach for climate change experiments that can be adopted in other seasonally snow-covered ecosystems to simulate expected changes resulting from global air temperature rise.
Precipitation amount and seasonal timing determine the duration and distribution of water available for plant and microbial activity in the cold desert sagebrush steppe. In this study, we sought to ...determine if a sustained shift in the amount and timing of precipitation would affect soil microbial diversity, community composition, and soil carbon (C) storage. Field plots were irrigated (+200 mm) during the dormant or growing-season for 17 years. Microbial community responses were assessed over the course of a year at two depths (15–20 cm, 95–100 cm) by terminal restriction fragment length polymorphism (T-RFLP), along with co-occurring changes in plant cover and edaphic properties. Bacterial richness, Shannon Weaver diversity, and composition in shallow soils (15–20 cm) as well as evenness in deep soils (95–100 cm) differed across irrigation treatments during July. Irrigation timing affected fungal community diversity and community composition during the dormant season and most strongly in deep soils (95–100 cm). Dormant-season irrigation increased the ratio of shrubs to forbs and reduced soil C in shallow soils by 16% relative to ambient conditions. It is unclear whether or not soil C will continue to decline with continued treatment application or if microbial adaptation could mitigate sustained soil C losses. Future changes in precipitation timing will affect soil microbes in a seasonally dependent manner and be coupled to co-varying effects of water content on vegetation and soil C.
•We manipulated precipitation timing for 17 years in the North American cold desert.•Co-occurring changes in microbial communities, vegetation, and soil C were assessed.•Bacteria were affected by growing season irrigation in shallow soils.•Fungi were affected by dormant season irrigation in deep soils.•Dormant season irrigation reduced soil C by 16% in shallow soils.
Northern forest ecosystems are projected to experience warmer growing seasons and increased soil freeze–thaw cycles in winter over the next century. Past studies show that warmer soils in the growing ...season enhance nitrogen uptake by plants, while soil freezing in winter reduces plant uptake and ecosystem retention of nitrogen, yet the combined effects of these changes on plant root capacity to take up nitrogen are unknown. We conducted a 2-year (2014–2015) experiment at Hubbard Brook Experimental Forest in New Hampshire, USA to characterize the response of root damage, nitrogen uptake capacity, and soil solution nitrogen to growing season warming combined with soil freeze–thaw cycles in winter. Winter freeze–thaw cycles damaged roots, reduced nitrogen uptake capacity by 42%, and increased soil solution ammonium in the early growing season (May–June). During the peak growing season (July), root nitrogen uptake capacity was reduced 40% by warming alone and 49% by warming combined with freeze–thaw cycles. These results indicate the projected combination of colder soils in winter and warmer soils in the snow-free season will alter root function by reducing root nitrogen uptake capacity and lead to transient increases of nitrogen in soil solution during the early growing season, with the potential to alter root competition for soil nitrogen and seasonal patterns of soil nitrogen availability. We conclude that considering interactive effects of changes in climate during winter and the snow-free season is essential for accurate determination of the response of nitrogen cycling in the northern hardwood forest to climate change.
Snow cover is projected to decline during the next century in many ecosystems that currently experience a seasonal snowpack. Because snow insulates soils from frigid winter air temperatures, soils ...are expected to become colder and experience more winter soil freezethaw cycles as snow cover continues to decline. Tree roots are adversely affected by snowpack reduction, but whether loss of snow will affect root-microbe interactions remains largely unknown. The objective of this study was to distinguish and attribute direct (e.g., winter snowand/or soil frost-mediated) vs. indirect (e.g., root-mediated) effects of winter climate change on microbial biomass, the potential activity of microbial exoenzymes, and net N mineralization and nitrification rates. Soil cores were incubated in situ in nylon mesh that either allowed roots to grow into the soil core (2 mm pore size) or excluded root ingrowth (50 µm pore size) for up to 29 months along a natural winter climate gradient at Hubbard Brook Experimental Forest, NH (USA). Microbial biomass did not differ among ingrowth or exclusion cores. Across sampling dates, the potential activities of cellobiohydrolase, phenol oxidase, and peroxidase, and net N mineralization rates were more strongly related to soil volumetric water content (P < 0.05; R² = 0.25-0.46) than to root biomass, snow or soil frost, or winter soil temperature (R² < 0.10). Root ingrowth was positively related to soil frost (P < 0.01; R² = 0.28), suggesting that trees compensate for overwinter root mortality caused by soil freezing by re-allocating resources towards root production. At the sites with the deepest snow cover, root ingrowth reduced nitrification rates by 30% (P < 0.01), showing that tree roots exert significant influence over nitrification, which declines with reduced snow cover. If soil freezing intensifies over time, then greater compensatory root growth may reduce nitrification rates directly via plantmicrobe N competition and indirectly through a negative feedback on soil moisture, resulting in lower N availability to trees in northern hardwood forests.
Soil microbial biomass can reach its annual maximum pool size beneath the winter snowpack and is known to decline abruptly following snowmelt in seasonally snow-covered ecosystems. Observed ...differences in winter versus summer microbial taxonomic composition also suggests that phylogenetically conserved traits may permit winter- versus summer-adapted microorganisms to occupy distinct niches. In this study, we sought to identify archaea, bacteria, and fungi that are associated with the soil microbial bloom overwinter and the subsequent biomass collapse following snowmelt at a high-altitude watershed in central Colorado, United States. Archaea, bacteria, and fungi were categorized into three life strategies (Winter-Adapted, Snowmelt-Specialist, Spring-Adapted) based upon changes in abundance during winter, the snowmelt period, and after snowmelt in spring. We calculated indices of phylogenetic relatedness (archaea and bacteria) or assigned functional attributes (fungi) to organisms within life strategies to infer whether phylogenetically conserved traits differentiate Winter-Adapted, Snowmelt-Specialist, and Spring-Adapted groups. We observed that the soil microbial bloom was correlated in time with a pulse of snowmelt infiltration, which commenced 65 days prior to soils becoming snow-free. A pulse of nitrogen (N, as nitrate) occurred after snowmelt, along with a collapse in the microbial biomass pool size, and an increased abundance of nitrifying archaea and bacteria (e.g., Thaumarchaeota, Nitrospirae). Winter- and Spring-Adapted archaea and bacteria were phylogenetically clustered, suggesting that phylogenetically conserved traits allow Winter- and Spring-Adapted archaea and bacteria to occupy distinct niches. In contrast, Snowmelt-Specialist archaea and bacteria were phylogenetically overdispersed, suggesting that the key mechanism(s) of the microbial biomass crash are likely to be density-dependent (e.g., trophic interactions, competitive exclusion) and affect organisms across a broad phylogenetic spectrum. Saprotrophic fungi were the dominant functional group across fungal life strategies, however, ectomycorrhizal fungi experienced a large increase in abundance in spring. If well-coupled plant-mycorrhizal phenology currently buffers ecosystem N losses in spring, then changes in snowmelt timing may alter ecosystem N retention potential. Overall, we observed that snowmelt separates three distinct soil niches that are occupied by ecologically distinct groups of microorganisms. This ecological differentiation is of biogeochemical importance, particularly with respect to the mobilization of nitrogen during winter, before and after snowmelt.
Climate models project higher growing-season temperatures and a decline in the depth and duration of winter snowpack throughout many north temperate ecosystems over the next century. A smaller ...snowpack is projected to induce more frequent soil freeze/thaw cycles in winter in northern hardwood forests of the northeastern United States. We measured the combined effects of warmer growing-season soil temperatures and increased winter freeze/thaw cycles on rates of leaf-level photosynthesis and transpiration (sap flow) of red maple (Acer rubrum) trees in a northern hardwood forest at the Climate Change Across Seasons Experiment at Hubbard Brook Experimental Forest in New Hampshire. Soil temperatures were warmed 5°C above ambient temperatures during the growing season and soil freeze/thaw cycles were induced in winter to mimic the projected changes in soil temperature over the next century. Relative to reference plots, growing-season soil warming increased rates of leaf-level photosynthesis by up to 85.32 ± 4.33%, but these gains were completely offset by soil freeze/thaw cycles in winter, suggesting that increased freeze/thaw cycles in winter over the next 100 yr will reduce the effect of warming on leaf-level carbon gains. Soil warming in the growing season increased rates of transpiration per kilopascal of vapor pressure deficit (VPD) by up to 727.39 ± 0.28%, even when trees were exposed to increased frequency of soil freeze/thaw cycles in the previous winter, which could influence regional hydrology in the future. Using climate projections downscaled from the Coupled Model Intercomparison Project, we project increased rates of whole-season transpiration in these forests over the next century by 42–61%. We also project 52–77 additional days when daily air temperatures will be above the long-term average daily maximum during the growing season at Hubbard Brook. Together, these results show that projected changes in climate across both the growing season and winter are likely to cause greater rates of water uptake and have no effect on rates of leaf-level carbon uptake by trees, with potential ecosystem consequences for hydrology and carbon cycling in northern hardwood forests.
Abstract
Background
Viruses impact nearly all organisms on Earth, including microbial communities and their associated biogeochemical processes. In soils, highly diverse viral communities have been ...identified, with a global distribution seemingly driven by multiple biotic and abiotic factors, especially soil temperature and moisture. However, our current understanding of the stability of soil viral communities across time and their response to strong seasonal changes in environmental parameters remains limited. Here, we investigated the diversity and activity of environmental soil DNA and RNA viruses, focusing especially on bacteriophages, across dynamics’ seasonal changes in a snow-dominated mountainous watershed by examining paired metagenomes and metatranscriptomes.
Results
We identified a large number of DNA and RNA viruses taxonomically divergent from existing environmental viruses, including a significant proportion of fungal RNA viruses, and a large and unsuspected diversity of positive single-stranded RNA phages (
Leviviricetes
), highlighting the under-characterization of the global soil virosphere. Among these, we were able to distinguish subsets of active DNA and RNA phages that changed across seasons, consistent with a “seed-bank” viral community structure in which new phage activity, for example, replication and host lysis, is sequentially triggered by changes in environmental conditions. At the population level, we further identified virus-host dynamics matching two existing ecological models: “Kill-The-Winner” which proposes that lytic phages are actively infecting abundant bacteria, and “Piggyback-The-Persistent” which argues that when the host is growing slowly, it is more beneficial to remain in a dormant state. The former was associated with summer months of high and rapid microbial activity, and the latter with winter months of limited and slow host growth.
Conclusion
Taken together, these results suggest that the high diversity of viruses in soils is likely associated with a broad range of host interaction types each adapted to specific host ecological strategies and environmental conditions. As our understanding of how environmental and host factors drive viral activity in soil ecosystems progresses, integrating these viral impacts in complex natural microbiome models will be key to accurately predict ecosystem biogeochemistry.
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