Fungal communities and their association with nitrogen-fixing bacteria affect early decomposition of Norway spruce deadwood

Gómez-Brandòn, María; Probst, Maraike; Siles, J.A.; Peintner, Ursula; Bardelli, Tommaso; Egli, Markus; Insam, Heribert; Ascher‐Jenull, Judith

doi:10.1038/s41598-020-64808-5

Cited by 42 publications

(42 citation statements)

References 57 publications

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“…As fungi and prokaryotes share the same habitat, they inevitably interact with each other (25). Knowledge about these interactions is rather rare, but evidence exists for links between N-fixing bacteria and fungi (38,42) or for fungal manipulation on prokaryotic growth (43,44). Although it seems obvious that colonization of fungal and prokaryotic species and thus the topology of networks are affected by their interactions, this was beyond the scope of the current analysis.…”

Section: Discussionmentioning

confidence: 93%

Amplicon Sequencing-Based Bipartite Network Analysis Confirms a High Degree of Specialization and Modularity for Fungi and Prokaryotes in Deadwood

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Fungi and prokaryotes are dominant colonizers of wood and mediate its decomposition. Much progress has been achieved to unravel these communities and link them to specific wood properties. However, comparative studies considering both groups of organisms and assessing their relationships to wood resources are largely missing. Bipartite interaction networks provide an opportunity to investigate this colonizer-resource relationship more in detail and aim to directly compare results between different biotic groups. The main questions were as follows. Are network structures reflecting the trophic relationship between fungal and prokaryotic colonizers and their resources? If so, do they reflect the critical role of these groups, especially that of fungi, during decomposition? We used amplicon sequencing data to analyze fungal and prokaryotic interaction networks from deadwood of 13 temperate tree species at an early to middle stage of decomposition. Several diversity- and specialization-related indices were determined and the observed network structures were related to intrinsic wood traits. We hypothesized nonrandom bipartite networks for both groups and a higher degree of specialization for fungi, as they are the key players in wood decomposition. The results reveal highly modular and specialized interaction networks for both groups of organisms, demonstrating that many fungi and prokaryotes are resource-specific colonizers. However, as the level of specialization of fungi significantly surpassed that of prokaryotes, our findings reflect the strong association between fungi and their host. Our novel approach shows that the application of bipartite interaction networks is a useful tool to explore, quantify, and compare the deadwood-colonizers relationship based on sequencing data. IMPORTANCE Deadwood is important for our forest ecosystems. It feeds and houses many organisms, e.g., fungi and prokaryotes, with many different species contributing to its decomposition and nutrient cycling. The aim of this study was to explore and quantify the relationship between these two main wood-inhabiting organism groups and their corresponding host trees. Two independent DNA-based amplicon sequencing data sets (fungi and prokaryotes) were analyzed via bipartite interaction networks. The links in the networks represent the interactions between the deadwood colonizers and their deadwood hosts. The networks allowed us to analyze whether many colonizing species interact mostly with a restricted number of deadwood tree species, so-called specialization. Our results demonstrate that many prokaryotes and fungi are resource-specific colonizers. The direct comparison between both groups revealed significantly higher specialization values for fungi, emphasizing their strong association to respective host trees, which reflects their dominant role in exploiting this resource.

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Section: Discussionmentioning

confidence: 93%

Amplicon Sequencing-Based Bipartite Network Analysis Confirms a High Degree of Specialization and Modularity for Fungi and Prokaryotes in Deadwood

Moll

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Bässler

et al. 2021

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“…The joint movement of bacteria with fungi (and hence, their interactions) might have deep consequences for deadwood decomposition and forest nutrient dynamics. Previous findings on co-occurrence patterns between wood-decaying fungi and N 2 -fixing bacteria suggest that deadwood decomposition might be an interactive process where bacteria may provide the N source and fungi provide the C source ( 10 , 11 , 28 , 36 ). Similar interactions between fungi and bacteria have also been reported in the process of litter decomposition ( 38 ).…”

Section: Discussionmentioning

confidence: 98%

“…Fungi are the main contributors to wood decomposition and deeply modify its physical structure ( 8 ); thus, deadwood decomposition in forest ecosystems has been traditionally attributed to wood-decaying fungi. Nevertheless, the role of bacteria, either directly or through interactions with fungi, is being increasingly recognized ( 8 – 10 ). There are innumerable mechanisms by which fungi can affect bacteria and bacteria can affect fungi during wood decomposition, and studying them separately completely neglects such interactive effects ( 11 ).…”

Section: Introductionmentioning

confidence: 99%

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Fungal Communities Are Important Determinants of Bacterial Community Composition in Deadwood

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Fungal-bacterial interactions play a key role in the functioning of many ecosystems. Thus, understanding their interactive dynamics is of central importance for gaining predictive knowledge on ecosystem functioning. However, it is challenging to disentangle the mechanisms behind species associations from observed co-occurrence patterns, and little is known about the directionality of such interactions. Here, we applied joint species distribution modeling to high-throughput sequencing data on co-occurring fungal and bacterial communities in deadwood to ask whether fungal and bacterial co-occurrences result from shared habitat use (i.e., deadwood’s properties) or whether there are fungal-bacterial interactive associations after habitat characteristics are taken into account. Moreover, we tested the hypothesis that the interactions are mainly modulated through fungal communities influencing bacterial communities. For that, we quantified how much the predictive power of the joint species distribution models for bacterial and fungal community improved when accounting for the other community. Our results show that fungi and bacteria form tight association networks (i.e., some species pairs co-occur more frequently and other species pairs co-occur less frequently than expected by chance) in deadwood that include common (or opposite) responses to the environment as well as (potentially) biotic interactions. Additionally, we show that information about the fungal occurrences and abundances increased the power to predict the bacterial abundances substantially, whereas information about the bacterial occurrences and abundances increased the power to predict the fungal abundances much less. Our results suggest that fungal communities may mainly affect bacteria in deadwood. IMPORTANCE Understanding the interactive dynamics between fungal and bacterial communities is important to gain predictive knowledge on ecosystem functioning. However, little is known about the mechanisms behind fungal-bacterial associations and the directionality of species interactions. Applying joint species distribution modeling to high-throughput sequencing data on co-occurring fungal-bacterial communities in deadwood, we found evidence that nonrandom fungal-bacterial associations derive from shared habitat use as well as (potentially) biotic interactions. Importantly, the combination of cross-validations and conditional cross-validations helped us to answer the question about the directionality of the biotic interactions, providing evidence that suggests that fungal communities may mainly affect bacteria in deadwood. Our modeling approach may help gain insight into the directionality of interactions between different components of the microbiome in other environments.

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“…The role of bacterial communities in the deadwood habitat is still underexplored compared to fungi ( Johnston et al, 2016 , 2019 ; Gómez-Brandón et al, 2020 ). Yet, the variations among bacterial communities within and between decay stages are poorly studied, as previously emphasized ( Hoppe et al, 2015 ; Kielak et al, 2016b ; Lee et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

The Molecular Information About Deadwood Bacteriomes Partly Depends on the Targeted Environmental DNA

et al. 2021

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Microbiome studies mostly rely on total DNA extracts obtained directly from environmental samples. The total DNA consists of both intra- and extracellular DNA, which differ in terms of their ecological interpretation. In the present study, we have investigated for the first time the differences among the three DNA types using microbiome sequencing of Picea abies deadwood logs (Hunter decay classes I, III, and V). While the bacterial compositions of all DNA types were comparable in terms of more abundant organisms and mainly depended on the decay class, we found substantial differences between DNA types with regard to less abundant amplicon sequence variants (ASVs). The analysis of the sequentially extracted intra- and extracellular DNA fraction, respectively, increased the ecological depth of analysis compared to the directly extracted total DNA pool. Both DNA fractions were comparable in proportions and the extracellular DNA appeared to persist in the P. abies deadwood logs, thereby causing its masking effect. Indeed, the extracellular DNA masked the compositional dynamics of intact cells in the total DNA pool. Our results provide evidence that the choice of DNA type for analysis might benefit a study’s answer to its respective ecological question. In the deadwood environment researched here, the differential analysis of the DNA types underlined the relevance of Burkholderiales, Rhizobiales and other taxa for P. abies deadwood decomposition and revealed that the role of Acidobacteriota under this scenario might be underestimated, especially compared to Actinobacteriota.

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Fungal communities and their association with nitrogen-fixing bacteria affect early decomposition of Norway spruce deadwood

Cited by 42 publications

References 57 publications

Amplicon Sequencing-Based Bipartite Network Analysis Confirms a High Degree of Specialization and Modularity for Fungi and Prokaryotes in Deadwood

Amplicon Sequencing-Based Bipartite Network Analysis Confirms a High Degree of Specialization and Modularity for Fungi and Prokaryotes in Deadwood

Fungal Communities Are Important Determinants of Bacterial Community Composition in Deadwood

The Molecular Information About Deadwood Bacteriomes Partly Depends on the Targeted Environmental DNA

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