Sulfide alters microbial functional potential in a methane and nitrogen cycling biofilm reactor

Abstract

Cross-feeding of metabolites between coexisting cells leads to complex and interconnected elemental cycling and microbial interactions. These relationships influence overall community function and can be altered by changes in substrate availability. Here, we used isotopic rate measurements and metagenomic sequencing to study how cross-feeding relationships changed in response to stepwise increases of sulfide concentrations in a membraneaerated biofilm reactor that was fed with methane and ammonium. Results showed that sulfide: (i) decreased nitrite oxidation rates but increased ammonia oxidation rates; (ii) changed the denitrifying community and increased nitrous oxide production; and (iii) induced dissimilatory nitrite reduction to ammonium (DNRA). We infer that inhibition of nitrite oxidation resulted in higher nitrite availability for DNRA, anammox, and nitrite-dependent anaerobic methane oxidation. In other words, sulfide likely disrupted microbial cross-feeding between AOB and NOB and induced cross-feeding between AOB and nitrite reducing organisms. Furthermore, these cross-feeding relationships were spatially distributed between biofilm and planktonic phases of the reactor. These results indicate that using sulfide as an electron donor will promote N 2 O and ammonium production, which is generally not desirable in engineered systems.

Difference and Network Analysis of Functional Genes Revealed the Hot Area of Carbon Degradation, Nitrogen, Phosphorus, and Sulfur Cycling in Blending Systems with Pyrite and Poly(3-hydroxybutyrate-hydroxyvalerate) for Nitrogen and Phosphorus Removal

“…Recently, 16S rRNA genes have been widely used to clarify the microbial community structure. Due to the metabolic flexibility of the mixotrophic denitrification process, the 16S rRNA genes are insufficient for determining the key players in the carbon, nitrogen, sulfur, and iron cycles . High-resolution methods are needed to resolve these coupled biogeochemical cycles .…”

Unraveling Nitrogen, Sulfur, and Carbon Metabolic Pathways and Microbial Community Transcriptional Responses to Substrate Deprivation and Toxicity Stresses in a Bioreactor Mimicking Anoxic Brackish Coastal Sediment Conditions

“…However, given that most microorganisms are widespread and functionally redundant, they are frequently treated as a “black box” in models—preventing the effective modeling of their reactions and responses. Additionally, recent efforts with laboratory cultures and engineered systems have provided insights about impacts of substrate availability changes on environmentally and economically relevant microbial communities ( Chen et al, 2017 ; Saad et al, 2017 ; Caffrey et al, 2019 ; Delgado Vela et al, 2021 ; Deng et al, 2021 ; Nie et al, 2021 ). Yet, few studies have examined microbial community responses to prolonged periods of substrate scarcity or environmental stresses in controlled systems ( Bürgmann et al, 2011 ; Shade et al, 2012 ).…”

“…For instance, Deng et al (2021) proposed that sulfide-driven partial denitrification could be coupled to anaerobic ammonium oxidation (anammox) in future applications, given that rapid oxidation of sulfide to elemental sulfur can prevent toxicity and inhibition of anammox activity. On the other hand, sulfide addition in a controlled aerated bioreactor setting promoted undesirable production of nitrous oxide and nitrite via partial denitrification and dissimilatory nitrite reduction to ammonium (DNRA), respectively ( Delgado Vela et al, 2021 ). These observations indicate that further studies are necessary to understand complex microbial community interactions and to evaluate how they can be best employed in biotechnological applications.…”

Unraveling nitrogen, sulfur and carbon metabolic pathways and microbial community transcriptional responses to substrate deprivation and toxicity stresses in a bioreactor mimicking anoxic brackish coastal sediment conditions

“…However, given that most microorganisms are widespread and functionally redundant, they are frequently treated as a “black box” in models - preventing the effective modeling of their reactions and responses. Additionally, recent efforts with laboratory cultures and engineered systems have obtained insights about impacts of substrate availability changes on environmentally and economically relevant microbial communities (9–14). Yet, few studies have examined microbial community responses to prolonged periods of substrate scarcity or environmental stresses in controlled systems (15, 16).…”

“…For instance, Deng et al proposed that sulfide-driven partial denitrification could be coupled to anaerobic ammonium oxidation (anammox) in future applications, given that rapid oxidation of sulfide to elemental sulfur can prevent toxicity and inhibition of anammox activity (13). On the other hand, sulfide addition in a controlled aerated bioreactor setting promoted undesirable production of nitrous oxide and nitrite via partial denitrification and dissimilatory nitrite reduction to ammonium (DNRA), respectively (14). These observations indicate that further studies are necessary to understand complex microbial community interactions and to evaluate how they can be best employed in biotechnological applications.…”