Iron controls the assembly processes of heterotrophic denitrifying microbial communities

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ORIGINAL PAPER

Iron controls the assembly processes of heterotrophic denitrifying microbial communities Ying Liu1 · Yizhi Sheng2,3  Received: 1 June 2020 / Accepted: 23 September 2020 © Springer Nature Switzerland AG 2020

Abstract Knowledge of the behavior of microbial communities in ecosystems is limited, yet microbes control partly all element cycles and, in turn, processes influencing pollution and climate change. In particular, heterotrophic denitrification is major process controlling the transformation of nitrogen oxides pollutants, e.g. nitrates (­ NO4-) and nitrous oxide (­ N2O), a greenhouse gas. Iron acts as either nutrient or stress in denitrifying microbial communities, yet underlying mechanisms are unclear. We hypothesized that iron plays a vital role in the assembly process of heterotrophic denitrifying microbial communities. To test this hypothesis we cultivated 17 microcosms under carbon- and iron-rich conditions. Geochemical analysis, 16S rRNA gene high-throughput sequencing, and multivariate statistical analysis were implemented to unravel the driving forces that shape the assembly process of microbial communities. Results reveal that iron was the most dominant factor influencing the diversity and composition of heterotrophic denitrifying communities, versus pH, C/N, temperature, nitrate reduction, and iron oxidation rates. Higher Fe concentration induced more clustered microbial interactions. Heterotrophic microbial community assembly is shaped by 90% stochastic processes, whereas deterministic processes rose with Fe(II) concentration. Overall our findings demonstrate that iron controls the balance between the deterministic and stochastic processes of heterotrophic denitrifying microbial communities. These mechanisms may have implications for bioremediation strategies. Keywords  Iron · Nitrate reduction · Groundwater · Microbial community · Denitrification · Assembly process

Introduction Iron is one of the ubiquitously abundant and redox-active transition metal elements on earth (Melton et  al. 2014; Weber et al. 2006). Nitrate, a widely distributed contaminant, is commonly eliminated from the aquatic environment via denitrification mediated by denitrifying microbial communities (Rivett et al. 2008; Wiszniowski et al. 2006). Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1031​1-020-01104​-8) contains supplementary material, which is available to authorized users. * Yizhi Sheng [email protected] 1



The Key Laboratory of Orogenic Belts and Crustal Evolution, School of Earth and Space Sciences, Peking University, Beijing 100871, China

2



Department of Geology and Environmental Earth Science, Miami University, Oxford, OH 45056, USA

3

School of Environment, Tsinghua University, Beijing 100084, China



In pristine or contaminated aquifers (Pathak and Hiratsuka 2010; Rivett et al. 2008) and groundwater bioremediation systems (Liu et al. 2016, 2018; Shakya et al. 2019; Sheng et al. 2017), Fe(II) can serve as an essential nutrient, electron