Transcriptomic evidences for microbial carbon and nitrogen cycles in the deoxygenated seawaters of Bohai Sea

Eutrophication-induced water deoxygenation occurs continually in coastal oceans, and alters community structure, metabolic processes, and the energy shunt, resulting in a major threat to the ecological environment. Seasonal deoxygenation events have occurred in the Bohai Sea (China), however, how these affect the functional activity of microorganisms remains unclear. Here, through the use of absolute quantification of 16S rRNA genes amplicon sequencing and metatranscriptomics approaches, we investigated the structure of the microbial community and the patterns of transcriptional activity in deoxygenated seawaters. The dominant phyla were Proteobacteria (average value, 1.4 × 10⁶ copies ml^-1), Cyanobacteria (3.7 × 10⁵ copies ml^-1), Bacteroidetes (2.7 × 10⁵ copies ml^-1), and the ammonia-oxidizing archaea Thaumarchaeota (1.9 × 10⁵ copies ml^-1). Among the various environmental factors, dissolved oxygen, pH and temperature displayed the most significant correlation with microbial community composition and functional activity. Metatranscriptomic data showed high transcriptional activity of Thaumarchaeota in the deoxygenated waters, with a significant increase in the expression of core genes representing ammonia oxidation, ammonia transport, and carbon fixation (3-hydroxypropionic acid/4-hydroxybutyric acid cycle) pathways. The transcripts of Cyanobacteria involved in photosynthesis and carbon fixation (Calvin-Benson-Bassham cycle) significantly decreased in low oxygen waters. Meanwhile, the transcripts for the ribulose bisphosphate carboxylase-encoding gene shifted from being assigned to photoautotrophic to chemoautotrophic organisms in surface and bottom waters, respectively. Moreover, the transcription profile indicated that heterotrophs play a critical role in transforming low-molecular-weight dissolved organic nitrogen. Elevated abundances of transcripts related to microbial antioxidant activity corresponded to an enhanced aerobic metabolism of Thaumarchaeota in the low oxygen seawater. In general, our transcriptional evidences showed a population increase of Thaumarchaeota, especially the coastal ecotype of ammonia oxidizers, in low oxygen aquatic environments, and indicated an enhanced contribution of chemolithoautotrophic carbon fixation to carbon flow.