Yu Han1, Nianzhi Jiao1, Yao Zhang1, Fan Zhang2, Chen He3, Xuejiao Liang1, Ruanhong Cai1, Quan Shi3, Kai Tang4. 1. State Key Laboratory of Marine Environmental Science, Fujian Key Laboratory of Marine Carbon Sequestration, College of Ocean and Earth Sciences, Xiamen University, Xiamen, 361102, People's Republic of China. 2. Department of Molecular Virology & Microbiology, Center for Metagenomics and Microbiome Research, Baylor College of Medicine, Houston, TX, 77030, USA. 3. State Key Laboratory of Heavy Oil Processing, China University of Petroleum (Beijing), Beijing, 102249, People's Republic of China. 4. State Key Laboratory of Marine Environmental Science, Fujian Key Laboratory of Marine Carbon Sequestration, College of Ocean and Earth Sciences, Xiamen University, Xiamen, 361102, People's Republic of China. tangkai@xmu.edu.cn.
Abstract
BACKGROUND: Phytoplankton blooms are frequent events in coastal areas and increase the production of organic matter that initially shapes the growth of opportunistic heterotrophic bacteria. However, it is unclear how these opportunists are involved in the transformation of dissolved organic matter (DOM) when blooms occur and the subsequent impacts on biogeochemical cycles. RESULTS: We used a combination of genomic, proteomic, and metabolomic approaches to study bacterial diversity, genome traits, and metabolic responses to assess the source and lability of DOM in a spring coastal bloom of Akashiwo sanguinea. We identified molecules that significantly increased during bloom development, predominantly belonging to amino acids, dipeptides, lipids, nucleotides, and nucleosides. The opportunistic members of the bacterial genera Polaribacter, Lentibacter, and Litoricola represented a significant proportion of the free-living and particle-associated bacterial assemblages during the stationary phase of the bloom. Polaribacter marinivivus, Lentibacter algarum, and Litoricola marina were isolated and their genomes exhibited streamlining characterized by small genome size and low GC content and non-coding densities, as well as a smaller number of transporters and peptidases compared to closely related species. However, the core proteomes identified house-keeping functions, such as various substrate transporters, peptidases, motility, chemotaxis, and antioxidants, in response to bloom-derived DOM. We observed a unique metabolic signature for the three species in the utilization of multiple dissolved organic nitrogen compounds. The metabolomic data showed that amino acids and dipeptides (such as isoleucine and proline) were preferentially taken up by P. marinivivus and L. algarum, whereas nucleotides and nucleosides (such as adenosine and purine) were preferentially selected by L. marina. CONCLUSIONS: The results suggest that the enriched DOM in stationary phase of phytoplankton bloom is a result of ammonium depletion. This environment drives genomic streamlining of opportunistic bacteria to exploit their preferred nitrogen-containing compounds and maintain nutrient cycling. Video abstract.
BACKGROUND:Phytoplankton blooms are frequent events in coastal areas and increase the production of organic matter that initially shapes the growth of opportunistic heterotrophic bacteria. However, it is unclear how these opportunists are involved in the transformation of dissolved organic matter (DOM) when blooms occur and the subsequent impacts on biogeochemical cycles. RESULTS: We used a combination of genomic, proteomic, and metabolomic approaches to study bacterial diversity, genome traits, and metabolic responses to assess the source and lability of DOM in a spring coastal bloom of Akashiwo sanguinea. We identified molecules that significantly increased during bloom development, predominantly belonging to amino acids, dipeptides, lipids, nucleotides, and nucleosides. The opportunistic members of the bacterial genera Polaribacter, Lentibacter, and Litoricola represented a significant proportion of the free-living and particle-associated bacterial assemblages during the stationary phase of the bloom. Polaribacter marinivivus, Lentibacter algarum, and Litoricola marina were isolated and their genomes exhibited streamlining characterized by small genome size and low GC content and non-coding densities, as well as a smaller number of transporters and peptidases compared to closely related species. However, the core proteomes identified house-keeping functions, such as various substrate transporters, peptidases, motility, chemotaxis, and antioxidants, in response to bloom-derived DOM. We observed a unique metabolic signature for the three species in the utilization of multiple dissolved organicnitrogen compounds. The metabolomic data showed that amino acids and dipeptides (such as isoleucine and proline) were preferentially taken up by P. marinivivus and L. algarum, whereas nucleotides and nucleosides (such as adenosine and purine) were preferentially selected by L. marina. CONCLUSIONS: The results suggest that the enriched DOM in stationary phase of phytoplankton bloom is a result of ammonium depletion. This environment drives genomic streamlining of opportunistic bacteria to exploit their preferred nitrogen-containing compounds and maintain nutrient cycling. Video abstract.