Soil Organic Carbon Enrichment Triggers In Situ Nitrogen Interception by Phototrophic Biofilms at the Soil–Water Interface: From Regional Scale to Microscale

Abstract

Phototrophic biofilms are easy to grow at sediment/soil–water interfaces (SWIs) in shallow aquatic ecosystems and greatly impact nutrient biogeochemical cycles. However, the pathways by which they contribute to nitrogen interception and interact with sediment/soil remains largely unknown. Here, we conducted a field investigation in paddy fields in various regions of China and found that nitrogen immobilized in biofilm biomass significantly positively correlated with soil organic carbon (SOC) content. A microcosm experiment showed that this was due to increased bacterial and algal diversity, biomass accumulation, and inorganic nitrogen assimilation at high SOC, especially high dissolved organic carbon (DOC) levels. The metatranscriptomics results further verified that many KO groups of PSII, PSI, AP, and PC in antenna proteins and glutamate synthesis were distinctly expressed at elevated SOC and DOC levels. Our results elucidated the effects and possible pathways of how SOC enrichment triggers photosynthesis and nitrogen immobilization by phototrophic biofilms. The results will provide meaningful information for in situ nitrogen interception by using phototrophic biofilms at the SWI in human-made wetlands to change internal nitrogen cycling.

Periphytic biofilms function as a double‐edged sword influencing nitrogen cycling in paddy fields

“…Periphytic biofilm is essentially a microbial aggregate (Liu et al, 2019; Liu et al, 2021; Sun, Gao, Sun, et al, 2021), and understanding their diversity, composition, and function (e.g. N accumulation and transformation) is crucial for exploiting biofilms for sustainable rice production (Xiong & Lu, 2022).…”

“…Bioaccumulation is an important mechanism by which periphytic biofilms affect element cycling in paddy fields (Sun et al, 2022); therefore, periphytic biofilms act as temporary pools of some elements in paddy fields (Liu et al, 2019, 2021; Sun, Gao, Sun, et al, 2021). However, further evidence is required to understand the impact of biofilms on the N cycle in rice fields.…”

Phototrophic Biofilms Transform Soil-Dissolved Organic Matter Similarly Despite Compositional and Environmental Differences

“…We hypothesized that TOC and TN had direct and positive influence on relative abundances of lipid-, protein/amino sugar-like DOM compounds but negative influence on lignin- and tannin-like DOM compounds and indirect influence via EPS (conceptual models in Figure S2). , EPSs directly influence the DOM compound classes by increasing carbohydrate-, protein-, and amino acid-like compounds, and we hypothesized that this effect would get stronger with growing time. Before modeling, all the variables used for SEM were z-score-transformed to allow comparisons among multiple predictors and models.…”

“…In addition to soil physicochemical properties, microbes influence soil DOM composition . In the many types of soils that undergo periodic flooding and drying, phototrophic biofilms at the soil–water interface (SWI) may be an underappreciated driver of changes in soil DOM due to the overlook of functions of SWI in carbon cycling, such as CO 2 fixation, metabolite secretion, and biomass degradation product release. , Phototrophic biofilms composed of microalgae, bacteria, protozoa, and abiotic substances are ubiquitous in soils under long-period flooding conditions (e.g., >20 days), such as paddy soils. − During one growing season, the biomass of phototrophic biofilms in 1 ha of paddy fields could be 1 ton, with consequent impacts on carbon and nutrient forms and bioavailability changes. , Compared to the standing soil organic carbon (SOC) stock (51 ton SOC/ha in the top 30 cm soil), the biofilm biomass is small; however, growth of phototrophic biofilms is a complex process related to DOM transformation. , DOM provides carbon and energy for heterotrophic bacteria and the formation of phototrophic biofilms. , Meanwhile, phototrophic biofilms secrete metabolites, especially extracellular polymeric substances (EPSs), to the environment as they grow. Compared to the low EPS concentration in soil, the high EPS production by growing biofilms may significantly increase labile DOM, such as carbohydrate- and protein/amino sugar-like compounds. ,− Subsequent biomass decomposition of phototrophic biofilms resembles the addition of exogenous organic carbon to soil, such as from a fertilizer .…”

“…8,9 Compared to the standing soil organic carbon (SOC) stock (51 ton SOC/ha in the top 30 cm soil), 12 the biofilm biomass is small; however, growth of phototrophic biofilms is a complex process related to DOM transformation. 13,14 DOM provides carbon and energy for heterotrophic bacteria and the formation of phototrophic biofilms. 9,13 Meanwhile, phototrophic biofilms secrete metabolites, especially extracellular polymeric substances (EPSs), to the environment as they grow.…”