Interspecific Plant Interactions Reflected in Soil Bacterial Community Structure and Nitrogen Cycling in Primary Succession.

Joseph E Knelman,Janet S Prevéy,Emily B Graham,Patrick Kelly,Steve K Schmidt,Eran Hood,Michael S Robeson

doi:10.3389/fmicb.2018.00128

Abstract

Past research demonstrating the importance plant–microbe interactions as drivers of ecosystem succession has focused on how plants condition soil microbial communities, impacting subsequent plant performance and plant community assembly. These studies, however, largely treat microbial communities as a black box. In this study, we sought to examine how emblematic shifts from early successional Alnus viridus ssp. sinuata (Sitka alder) to late successional Picea sitchensis (Sitka spruce) in primary succession may be reflected in specific belowground changes in bacterial community structure and nitrogen cycling related to the interaction of these two plants. We examined early successional alder-conditioned soils in a glacial forefield to delineate how alders alter the soil microbial community with increasing dominance. Further, we assessed the impact of late-successional spruce plants on these early successional alder-conditioned microbiomes and related nitrogen cycling through a leachate addition microcosm experiment. We show how increasingly abundant alder select for particular bacterial taxa. Additionally, we found that spruce leachate significantly alters the composition of these microbial communities in large part by driving declines in taxa that are enriched by alder, including bacterial symbionts. We found these effects to be spruce specific, beyond a general leachate effect. Our work also demonstrates a unique influence of spruce on ammonium availability. Such insights bolster theory relating the importance of plant–microbe interactions with late-successional plants and interspecific plant interactions more generally.

Highlights

Building on long-standing perspectives that have examined ecosystem succession in terms of plant communities (Clements, 1916; Vitousek et al, 1993; Chapin et al, 1994), research is increasingly demonstrating the importance of soil microbial community succession in mediating both physical and chemical changes in ecosystem development (Nemergut et al, 2007; Schmidt et al, 2008; Interspecific Plant Interactions via MicrobiomeKnelman et al, 2014; Castle et al, 2017)
Increases in the prominence of Actinobacteria, Acidobacteria, Bacteroidetes, Planctomycetes, and Alphaproteobacteria occurred with increasing soil age and alder dominance (Table 2)
While the importance of alders in relation to plant community turnover and succession has been examined in the past (Chapin et al, 1994; Clein and Schimel, 1995; Schimel et al, 1996), research has not taken a high resolution view of how bacterial community structure of alder influenced soil changes over succession, or how interspecific interactions between these early alder soils and late successional spruce may occur via differential selection on bacterial community structure

Summary

Introduction

Building on long-standing perspectives that have examined ecosystem succession in terms of plant communities (Clements, 1916; Vitousek et al, 1993; Chapin et al, 1994), research is increasingly demonstrating the importance of soil microbial community succession in mediating both physical and chemical changes in ecosystem development (Nemergut et al, 2007; Schmidt et al, 2008; Interspecific Plant Interactions via MicrobiomeKnelman et al, 2014; Castle et al, 2017). Plants may exert species-specific effects on microbial communities through litter inputs, rhizodeposition, and the unique chemical and physical attributes of the root compartment (Bonito et al, 2014; Lebeis et al, 2015; Reinhold-Hurek et al, 2015; Lareen et al, 2016) Such microbial communities may feedback on plant communities through direct effects of plant-microbe symbioses and indirect effects via changes in microbial-mediated biogeochemistry (Van Der Heijden et al, 2008; Bever et al, 2010; Ke et al, 2015; Agler et al, 2016; Van Der Heijden and Hartmann, 2016). Beyond understanding how heterospecific plants condition soil microbial communities with implication for community assembly across succession, there remains a need to mechanistically describe how these interactions are being played out in soil bacterial community structure and related biogeochemistry at a higher resolution

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Discussion

Conclusion