Coupling Between Carbon and Nitrogen Metabolic Processes Mediated by Coastal Microbes in Synechococcus-Derived Organic Matter Addition Incubations

Rui Xie; Yu Wang; Qi Chen; Weidong Guo; Nianzhi Jiao; Qiang Zheng

doi:10.3389/fmicb.2020.01041

Coupling Between Carbon and Nitrogen Metabolic Processes Mediated by Coastal Microbes in Synechococcus-Derived Organic Matter Addition Incubations

Front Microbiol. 2020 May 25:11:1041. doi: 10.3389/fmicb.2020.01041. eCollection 2020.

Authors

Rui Xie^{1

2}, Yu Wang^{1

2

3}, Qi Chen^{1

2}, Weidong Guo^{1

4}, Nianzhi Jiao^{1

2}, Qiang Zheng^{1

2}

Affiliations

¹ State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, China.
² Fujian Key Laboratory of Marine Carbon Sequestration, Xiamen University, Xiamen, China.
³ College of Environment and Ecology, Xiamen University, Xiamen, China.
⁴ Key Laboratory of Coastal and Wetland Ecosystems, Ministry of Education, Xiamen University, Xiamen, China.

Abstract

Phytoplankton are major contributors to labile organic matter in the upper ocean. Diverse heterotrophic bacteria successively metabolize these labile compounds and drive elemental biogeochemical cycling. We investigated the bioavailability of Synechococcus-derived organic matter (SOM) by estuarine and coastal microbes during 180-day dark incubations. Variations in organic carbon, inorganic nutrients, fluorescent dissolved organic matter (FDOM), and total/active microbial communities were monitored. The entire incubations could be partitioned into three phases (labeled I, II, and III) based on the total organic carbon (TOC) consumption rates of 6.38-7.01, 0.53-0.64, and 0.10-0.13 μmol C L^-1 day^-1, respectively. This corresponded with accumulation processes of NH₄ ⁺, NO₂ ^-, and NO₃ ^-, respectively. One tryptophan-like (C1) and three humic-like (C2, C3, and C4) FDOM components were identified. The intensity variation of C1 followed bacterial growth activities, and C2, C3, and C4 displayed labile, semi-labile, and refractory DOM characteristics, respectively. Alphaproteobacteria, Gammaproteobacteria, Bacteroidetes, and Actinobacteria dominated the quickly consumed process of SOM (phase I) coupled with a substantial amount of NH₄ ⁺ generation. Thaumarchaeota became an abundant population with the highest activities in phase II, especially in the free-living size-fraction, and these organisms could perform chemoautotroph processes through the ammonia oxidation. Microbial populations frequently found in the dark ocean, even the deep sea, became abundant during phase III, in which Nitrospinae/Nitrospirae obtained energy through nitrite oxidation. Our results shed light on the transformation of different biological availability of organic carbon by coastal microorganisms which coupled with the regeneration of different form of inorganic nitrogen.

Keywords: Synechococcus-derived organic matter; fluorescent dissolved organic matter; heterotrophic bacteria; nitrogen cycling; recalcitrant dissolved organic matter.