Aerobic bacteria produce nitric oxide via denitrification and promote algal population collapse

被引:23
作者
Abada, Adi [1 ]
Beiralas, Roni [1 ]
Narvaez, Delia [1 ]
Sperfeld, Martin [1 ]
Duchin-Rapp, Yemima [1 ]
Lipsman, Valeria [1 ]
Yuda, Lilach [1 ]
Cohen, Bar [1 ]
Carmieli, Raanan [2 ]
Ben-Dor, Shifra [3 ]
Rocha, Jorge [4 ]
Huang Zhang, Irene [5 ]
Babbin, Andrew R. [5 ]
Segev, Einat [1 ]
机构
[1] Weizmann Inst Sci, Dept Plant & Environm Sci, Rehovot, Israel
[2] Weizmann Inst Sci, Dept Chem Res Support, Rehovot, Israel
[3] Weizmann Inst Sci, Dept Life Sci Core Facil, Rehovot, Israel
[4] CIDEA Consortium Conacyt, Ctr Invest Alimentac & Desarrollo, Hermosillo, Mexico
[5] MIT, Dept Earth Atmospher & Planetary Sci, Cambridge, MA USA
基金
欧洲研究理事会;
关键词
PROGRAMMED CELL-DEATH; PHAEOBACTER-INHIBENS; EMILIANIA-HUXLEYI; SP NOV; REDUCTASE; PHYTOPLANKTON; OXYGEN; GROWTH; NITRIFICATION; METABOLISM;
D O I
10.1038/s41396-023-01427-8
中图分类号
Q14 [生态学(生物生态学)];
学科分类号
071012 ; 0713 ;
摘要
Microbial interactions govern marine biogeochemistry. These interactions are generally considered to rely on exchange of organic molecules. Here we report on a novel inorganic route of microbial communication, showing that algal-bacterial interactions between Phaeobacter inhibens bacteria and Gephyrocapsa huxleyi algae are mediated through inorganic nitrogen exchange. Under oxygen-rich conditions, aerobic bacteria reduce algal-secreted nitrite to nitric oxide (NO) through denitrification, a well-studied anaerobic respiratory mechanism. The bacterial NO is involved in triggering a cascade in algae akin to programmed cell death. During death, algae further generate NO, thereby propagating the signal in the algal population. Eventually, the algal population collapses, similar to the sudden demise of oceanic algal blooms. Our study suggests that the exchange of inorganic nitrogen species in oxygenated environments is a potentially significant route of microbial communication within and across kingdoms.
引用
收藏
页码:1167 / 1183
页数:17
相关论文
共 114 条
[101]   The Ocean Gene Atlas: exploring the biogeography of plankton genes online [J].
Villar, Emilie ;
Vannier, Thomas ;
Vernette, Caroline ;
Lescot, Magali ;
Cuenca, Miguelangel ;
Alexandre, Aurelien ;
Bachelerie, Paul ;
Rosnet, Thomas ;
Pelletier, Eric ;
Sunagawa, Shinichi ;
Hingamp, Pascal .
NUCLEIC ACIDS RESEARCH, 2018, 46 (W1) :W289-W295
[102]   Nitric oxide signaling and transcriptional control of denitrification genes in Pseudomonas stutzeri [J].
Vollack, KU ;
Zumft, WG .
JOURNAL OF BACTERIOLOGY, 2001, 183 (08) :2516-2526
[103]   Environmental biology of the marine Roseobacter lineage [J].
Wagner-Doebler, Irene ;
Biebl, Hanno .
ANNUAL REVIEW OF MICROBIOLOGY, 2006, 60 :255-280
[104]   Sulfite Oxidase Catalyzes Single-Electron Transfer at Molybdenum Domain to Reduce Nitrite to Nitric Oxide [J].
Wang, Jun ;
Krizowski, Sabina ;
Fischer-Schrader, Katrin ;
Niks, Dimitri ;
Tejero, Jesus ;
Sparacino-Watkins, Courtney ;
Wang, Ling ;
Ragireddy, Venkata ;
Frizzell, Sheila ;
Kelley, Eric E. ;
Zhang, Yingze ;
Basu, Partha ;
Hille, Russ ;
Schwarz, Guenter ;
Gladwin, Mark T. .
ANTIOXIDANTS & REDOX SIGNALING, 2015, 23 (04) :283-294
[105]   Investigation of the Genetics and Biochemistry of Roseobacticide Production in the Roseobacter Clade Bacterium Phaeobacter inhibens [J].
Wang, Rurun ;
Gallant, Etienne ;
Seyedsayamdost, Mohammad R. .
MBIO, 2016, 7 (02)
[106]   NITRIFICATION AND NITRIC-OXIDE IN THE OXYGEN MINIMUM OF THE EASTERN TROPICAL NORTH PACIFIC [J].
WARD, BB ;
ZAFIRIOU, OC .
DEEP-SEA RESEARCH PART A-OCEANOGRAPHIC RESEARCH PAPERS, 1988, 35 (07) :1127-1142
[107]   Bacterial alkylquinolone signaling contributes to structuring microbial communities in the ocean [J].
Whalen, Kristen E. ;
Becker, Jamie W. ;
Schrecengost, Anna M. ;
Gao, Yongjie ;
Giannetti, Nicole ;
Harvey, Elizabeth L. .
MICROBIOME, 2019, 7 (1)
[108]   Global Response of Phaeobacter inhibens DSM 17395 to Deletion of Its 262-kb Chromid Encoding Antibiotic Synthesis [J].
Wuensch, Daniel ;
Strijkstra, Annemieke ;
Woehlbrand, Lars ;
Freese, Heike M. ;
Scheve, Sabine ;
Hinrichs, Christina ;
Trautwein, Kathleen ;
Maczka, Michael ;
Petersen, Joern ;
Schulz, Stefan ;
Overmann, Joerg ;
Rabus, Ralf .
MICROBIAL PHYSIOLOGY, 2020, 30 (1-6) :9-24
[109]   Denitrifying Alphaproteobacteria from the Arabian Sea That Express nosZ, the Gene Encoding Nitrous Oxide Reductase, in Oxic and Suboxic Waters [J].
Wyman, Michael ;
Hodgson, Sylvia ;
Bird, Clare .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2013, 79 (08) :2670-2681
[110]   Involvement of ethylene and nitric oxide in cell death in mastoparan-treated unicellular alga Chlamydomonas reinhardtii [J].
Yordanova, Zhenya P. ;
Lakimova, Elena T. ;
Cristescu, Simona M. ;
Harren, Frans J. M. ;
Kapchina-Toteva, Veneta M. ;
Woltering, Ernst J. .
CELL BIOLOGY INTERNATIONAL, 2010, 34 (03) :301-308