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ABSTRACT Bacteria are major drivers of organic matter decomposition and play crucial roles in global nutrient cycling. Although the degradation of dead fungal biomass (necromass) is increasingly recognized as an important contributor to soil carbon (C) and nitrogen (N) cycling, the genes and metabolic pathways involved in necromass degradation are less characterized. In particular, how bacteria degrade necromass containing different quantities of melanin, which largely control rates of necromass decompositionin situ, is largely unknown. To address this gap, we conducted a multi-timepoint transcriptomic analysis using three Gram-negative, bacterial species grown on low or high melanin necromass ofHyaloscypha bicolor. The bacterial species,Cellvibrio japonicus, Chitinophaga pinensis, andSerratia marcescens, belong to genera known to degrade necromassin situ. We found that while bacterial growth was consistently higher on low than high melanin necromass, the CAZyme-encoding gene expression response of the three species was similar between the two necromass types. Interestingly, this trend was not shared for genes encoding nitrogen utilization, which varied inC. pinensisandS. marcescensduring growth on high vs low melanin necromass. Additionally, this study tested the metabolic capabilities of these bacterial species to grow on a diversity of C and N sources and found that the three bacteria have substantially different utilization patterns. Collectively, our data suggest that as necromass changes chemically over the course of degradation, certain bacterial species are favored based on their differential metabolic capacities.IMPORTANCEFungal necromass is a major component of the carbon (C) in soils as well as an important source of nitrogen (N) for plant and microbial growth. Bacteria associated with necromass represent a distinct subset of the soil microbiome and characterizing their functional capacities is the critical next step toward understanding how they influence necromass turnover. This is particularly important for necromass varying in melanin content, which has been observed to control the rate of necromass decomposition across a variety of ecosystems. Here we assessed the gene expression of three necromass-degrading bacteria grown on low or high melanin necromass and characterized their metabolic capacities to grow on different C and N substrates. These transcriptomic and metabolic studies provide the first steps toward assessing the physiological relevance of up-regulated CAZyme-encoding genes in necromass decomposition and provide foundational data for generating a predictive model of the molecular mechanisms underpinning necromass decomposition by soil bacteria. 

ABSTRACT Dead fungal cells, known as necromass, are increasingly recognised as significant contributors to long‐term soil carbon pools, yet the genes involved in necromass decomposition are poorly understood. In particular, how microorganisms degrade necromass with differing initial cell wall chemical compositions using carbohydrate‐active enzymes (CAZymes) has not been well studied. Based on the frequent occurrence and high abundance of the fungal genusTrichodermaon decaying fungal necromass in situ, we grewTrichoderma reeseiRUT‐C30 on low and high melanin necromass ofHyaloscypha bicolor(Ascomycota) in liquid cultures and assessedT. reeseigene expression relative to each other and relative to glucose. Transcriptome data revealed thatT. reeseiup‐regulated many genes (over 100; necromass versus glucose substrate) coding for CAZymes, including enzymes that would target individual layers of an Ascomycota fungal cell wall. We also observed differential expression of protease‐ and laccase‐encoding genes on high versus low melanin necromass, highlighting a subset of genes (fewer than 15) possibly linked to the deconstruction of melanin, a cell wall constituent that limits necromass decay rates in nature. Collectively, these results advance our understanding of the genomic traits underpinning the rates and fates of carbon turnover in an understudied pool of Earth's belowground carbon, fungal necromass. 

Abstract Microbial necromass is increasingly recognized as an important fast‐cycling component of the long‐term carbon present in soils. To better understand how fungi and bacteria individually contribute to the decomposition of fungal necromass, three particle sizes (>500, 250–500, and <250 μm) ofHyaloscypha bicolornecromass were incubated in laboratory microcosms inoculated with individual strains of two fungi and two bacteria. Decomposition was assessed after 15 and 28 days via necromass loss, microbial respiration, and changes in necromass pH, water content, and chemistry. To examine how fungal–bacterial interactions impact microbial growth on necromass, single and paired cultures of bacteria and fungi were grown in microplates containing necromass‐infused media. Microbial growth was measured after 5 days through quantitative PCR. Regardless of particle size, necromass colonized by fungi had higher mass loss and respiration than both bacteria and uninoculated controls. Fungal colonization increased necromass pH, water content, and altered chemistry, while necromass colonized by bacteria remained mostly unaltered. Bacteria grew significantly more when co‐cultured with a fungus, while fungal growth was not significantly affected by bacteria. Collectively, our results suggest that fungi act as key early decomposers of fungal necromass and that bacteria may require the presence of fungi to actively participate in necromass decomposition. 

ABSTRACT Microbial necromass contributes significantly to both soil carbon (C) persistence and ecosystem nitrogen (N) availability, but quantitative estimates of C and N movement from necromass into soils and decomposer communities are lacking. Additionally, while melanin is known to slow fungal necromass decomposition, how it influences microbial C and N acquisition as well as elemental release into soils remains unclear. Here, we tracked decomposition of isotopically labeled low and high melanin fungal necromass and measured¹³C and¹⁵N accumulation in surrounding soils and microbial communities over 77 d in a temperate forest in Minnesota, USA. Mass loss was significantly higher from low melanin necromass, corresponding with greater¹³C and¹⁵N soil inputs. A taxonomically and functionally diverse array of bacteria and fungi was enriched in¹³C and/or¹⁵N at all sampling points, with enrichment being consistently higher on low melanin necromass and earlier in decomposition. Similar patterns of preferential C and N enrichment of many bacterial and fungal genera early in decomposition suggest that both microbial groups co-contribute to the rapid assimilation of resource-rich soil organic matter inputs. While overall richness of taxa enriched in C was higher than in N for both bacteria and fungi, there was a significant positive relationship between C and N in co-enriched taxa. Collectively, our results demonstrate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate but also necromass C and N release and that both elements are rapidly co-utilized by diverse bacterial and fungal decomposers in natural settings. IMPORTANCERecent studies indicate that microbial dead cells, particularly those of fungi, play an important role in long-term carbon persistence in soils. Despite this growing recognition, how the resources within dead fungal cells (also known as fungal necromass) move into decomposer communities and soils are poorly quantified, particularly in studies based in natural environments. In this study, we found that the contribution of fungal necromass to soil carbon and nitrogen availability was slowed by the amount of melanin present in fungal cell walls. Further, despite the overall rapid acquisition of carbon and nitrogen from necromass by a diverse range of both bacteria and fungi, melanization also slowed microbial uptake of both elements. Collectively, our results indicate that melanization acts as a key ecological trait mediating not only fungal necromass decomposition rate, but also necromass carbon and nitrogen release into soil as well as microbial resource acquisition. 

Abstract Despite growing interest in fungal necromass decomposition due to its importance in soil carbon retention, whether a consistent group of microorganisms is associated with decomposing necromass remains unresolved. Here, we synthesize knowledge on the composition of the bacterial and fungal communities present on decomposing fungal necromass from a variety of fungal species, geographic locations, habitats, and incubation times. We found that there is a core group of both bacterial and fungal genera (i.e. a core fungal necrobiome), although the specific size of the core depended on definition. Based on a metric that included both microbial frequency and abundance, we demonstrate that the core is taxonomically and functionally diverse, including bacterial copiotrophs and oligotrophs as well as fungal saprotrophs, ectomycorrhizal fungi, and both fungal and animal parasites. We also show that the composition of the core necrobiome is notably dynamic over time, with many core bacterial and fungal genera having specific associations with the early, middle, or late stages of necromass decomposition. While this study establishes the existence of a core fungal necrobiome, we advocate that profiling the composition of fungal necromass decomposer communities in tropical environments and other terrestrial biomes beyond forests is needed to fill key knowledge gaps regarding the global nature of the fungal necrobiome. 

Summary Dead fungal mycelium (necromass) represents a critical component of soil carbon (C) and nutrient cycles. Assessing how the microbial communities associated with decomposing fungal necromass change as global temperatures rise will help in determining how these belowground organic matter inputs contribute to ecosystem responses.In this study, we characterized the structure of bacterial and fungal communities associated with multiple types of decaying mycorrhizal fungal necromass incubated within mesh bags across a 9°C whole ecosystem temperature enhancement in a boreal peatland.We found major taxonomic and functional shifts in the microbial communities present on decaying mycorrhizal fungal necromass in response to warming. These changes were most pronounced in hollow microsites, which showed convergence towards the necromass‐associated microbial communities present in unwarmed hummocks. We also observed a high colonization of ericoid mycorrhizal fungal necromass by fungi from the same genera as the necromass.These results indicate that microbial communities associated with mycorrhizal fungal necromass decomposition are likely to change significantly with future climate warming, which may have strong impacts on soil biogeochemical cycles in peatlands. Additionally, the high enrichment of congeneric fungal decomposers on ericoid mycorrhizal necromass may help to explain the increase in ericoid shrub dominance in warming peatlands. 

Microbial community dynamics are dependent on interactions between the community members, yet studies of interactions across domains and with multiple experimental approaches are lacking. In this study, we explored interactions between bacteria and fungi associated with decaying fungal necromass using both field-based co-occurrence networks and laboratory-based pairwise interactions. The majority of field-derived bacterial-fungal correlations were negative, suggesting a potentially competitive environment within necromass compared to other systems. Laboratory experiments consisted of bacteria most often reducing fungal growth, while the fungal effect on bacterial growth was more varied and dependent on bacterial taxa. However, these interactions were not consistently predicted by field correlations, highlighting a disconnect between field-based and direct experimental approaches. Our findings suggest that using co-occurrence networks alone to predict BFI outcomes could be misleading, emphasizing the need for more comprehensive, multi-method studies to capture the dynamic and context-dependent nature of microbial interactions.