Invisible to the naked eye lies a tremendous diversity of organic molecules and organisms that make major contributions to important biogeochemical cycles. However, how the diversity and composition of these two communities are interlinked remains poorly characterized in fresh waters, despite the potential for chemical and microbial diversity to promote one another. Here we exploited gradients in chemodiversity within a common microbial pool to test how chemical and biological diversity covary and characterized the implications for ecosystem functioning. We found that both chemodiversity and genes associated with organic matter decomposition increased as more plant litterfall accumulated in experimental lake sediments, consistent with scenarios of future environmental change. Chemical and microbial diversity were also positively correlated, with dissolved organic matter having stronger effects on microbes than vice versa. Under our experimental scenarios that increased sediment organic matter from 5 to 25% or darkened overlying waters by 2.5 times, the resulting increases in chemodiversity could increase greenhouse gas concentrations in lake sediments by an average of 1.5 to 2.7 times, when all of the other effects of litterfall and water color were considered. Our results open a major new avenue for research in aquatic ecosystems by exposing connections between chemical and microbial diversity and their implications for the global carbon cycle in greater detail than ever before.

Global change is altering the vast amount of carbon cycled by microbes between land and freshwater, but how viruses mediate this process is poorly understood. Here, we show that viruses direct carbon cycling in lake sediments, and these impacts intensify with future changes in water clarity and terrestrial organic matter (tOM) inputs. Using experimental tOM gradients within sediments of a clear and a dark boreal lake, we identified 156 viral operational taxonomic units (vOTUs), of which 21% strongly increased with abundances of key bacteria and archaea, identified via metagenome-assembled genomes (MAGs). MAGs included the most abundant prokaryotes, which were themselves associated with dissolved organic matter (DOM) composition and greenhouse gas (GHG) concentrations. Increased abundances of virus-like particles were separately associated with reduced bacterial metabolism and with shifts in DOM toward amino sugars, likely released by cell lysis rather than higher molecular mass compounds accumulating from reduced tOM degradation. An additional 9.6% of vOTUs harbored auxiliary metabolic genes associated with DOM and GHGs. Taken together, these different effects on host dynamics and metabolism can explain why abundances of vOTUs rather than MAGs were better overall predictors of carbon cycling. Future increases in tOM quantity, but not quality, will change viral composition and function with consequences for DOM pools. Given their importance, viruses must now be explicitly considered in efforts to understand and predict the freshwater carbon cycle and its future under global environmental change.

Boreal lakes are major components of the global carbon cycle, partly because of sediment‐bound heterotrophic microorganisms that decompose within‐lake and terrestrially derived organic matter (t‐OM). The ability for sediment bacteria to break down and alter t‐OM may depend on environmental characteristics and community composition. However, the connection between these two potential drivers of decomposition is poorly understood. We tested how bacterial activity changed along experimental gradients in the quality and quantity of t‐OM inputs into littoral sediments of two small boreal lakes, a dark and a clear lake, and measured the abundance of operational taxonomic units and functional genes to identify mechanisms underlying bacterial responses. We found that bacterial production (BP) decreased across lakes with aromatic dissolved organic matter (DOM) in sediment pore water, but the process underlying this pattern differed between lakes. Bacteria in the dark lake invested in the energetically costly production of extracellular enzymes as aromatic DOM increased in availability in the sediments. By contrast, bacteria in the clear lake may have lacked the nutrients and/or genetic potential to degrade aromatic DOM and instead mineralized photo‐degraded OM into CO₂. The two lakes differed in community composition, with concentrations of dissolved organic carbon and pH differentiating microbial assemblages. Furthermore, functional genes relating to t‐OM degradation were relatively higher in the dark lake. Our results suggest that future changes in t‐OM inputs to lake sediments will have different effects on carbon cycling depending on the potential for photo‐degradation of OM and composition of resident bacterial communities.

Forests in the northeastern US are experiencing shifts in community composition due to the northward migration of warm-adapted tree species and certain species’ declines (for example, white ash and eastern hemlock) due to invasive insects. Changes in belowground fungal communities and associated functions will inevitably follow. Therefore, we sought to investigate the relative importance of two important tree characteristics—mycorrhizal type [ectomycorrhizal (EcM) or arbuscular mycorrhizal (AM)] and leaf habit (deciduous or evergreen) on soil fungal community composition and organic matter cycling. We sampled soil in the organic and mineral horizons beneath two AM-associated (Fraxinus americana and Thuja occidentalis) and two ECM-associated tree species (Betula alleghaniensis and Tsuga canadensis), with an evergreen and deciduous species in each mycorrhizal group. To characterize fungal communities and organic matter decomposition beneath each tree species, we sequenced the ITS1 region of fungal DNA and measured the potential activity of carbon- and nitrogen-targeting extracellular enzymes. Each tree species harbored distinct fungal communities, supporting the need to consider both mycorrhizal type and leaf habit. However, between tree characteristics, mycorrhizal type better predicted fungal communities. Across fungal guilds, saprotrophic fungi were the most important group in shaping fungal community differences in soils beneath all tree species. The effect of leaf habit on carbon- and nitrogen-targeting hydrolytic enzymes depended on tree mycorrhizal association in the organic horizon, while oxidative enzyme activities were higher beneath EcM-associated trees across both soil horizons and leaf habits.

Mycorrhizal fungi can affect soil organic matter cycling through several mechanisms including priming, nutrient competition, and direct enzyme production. Differences in nutrient foraging strategies between ectomycorrhizal (EcM) and arbuscular mycorrhizal (AM) fungi produce divergent belowground dynamics: where EcM can take up organic nitrogen and directly break down soil organic matter (SOM) by producing enzymes, AM fungi are limited to scavenging mineral N. EcM-associated tree species also have leaf litter with relatively higher ratios of carbon to nitrogen (C:N), and belowground saprotrophic communities more dominated by fungi. Consequently, free-living microbes in EcM-dominated soils should experience nitrogen limitation, with subsequent increases in enzyme production and decreased carbon use efficiency (CUE). However, the relative importance of the effects of substrate quality and fungal community composition on enzyme production and CUE are unclear. To assess this distinction, we sampled the organic horizon and 10 cm of the mineral horizon in northern temperate forest soils along a gradient of EcM dominance. We characterized fungal community composition by measuring EcM relative abundances from extracted fungal DNA and the fungal to bacterial (F:B) ratios from phospholipid fatty acid (PLFA) analysis. We assessed soil substrate quality as the soil C:N ratio. Soil microbial functions were measured as potential activities of five hydrolytic and two oxidative enzymes, and microbial CUE. We found that the fungal community, represented by either the F:B ratio, EcM relative abundance, or both, affected CUE and six measured enzyme activities, while the C:N ratio affected only oxidative and chitin-targeting extracellular enzyme activities. Our results highlight the use of EcM relative dominance as a predictor of soil microbial community composition and function independent of substrate quality.