PMID- 37775536 OWN - NLM STAT- MEDLINE DCOM- 20231204 LR - 20231217 IS - 1751-7370 (Electronic) IS - 1751-7362 (Print) IS - 1751-7362 (Linking) VI - 17 IP - 12 DP - 2023 Dec TI - Nitrogen transfer and cross-feeding between Azotobacter chroococcum and Paracoccus aminovorans promotes pyrene degradation. PG - 2169-2181 LID - 10.1038/s41396-023-01522-w [doi] AB - Nitrogen is a limiting nutrient for degraders function in hydrocarbon-contaminated environments. Biological nitrogen fixation by diazotrophs is a natural solution for supplying bioavailable nitrogen. Here, we determined whether the diazotroph Azotobacter chroococcum HN can provide nitrogen to the polycyclic aromatic hydrocarbon-degrading bacterium Paracoccus aminovorans HPD-2 and further explored the synergistic interactions that facilitate pyrene degradation in nitrogen-deprived environments. We found that A. chroococcum HN and P. aminovorans HPD-2 grew and degraded pyrene more quickly in co-culture than in monoculture. Surface-enhanced Raman spectroscopy combined with (15)N stable isotope probing (SERS - (15)N SIP) demonstrated that A. chroococcum HN provided nitrogen to P. aminovorans HPD-2. Metabolite analysis and feeding experiments confirmed that cross-feeding occurred between A. chroococcum HN and P. aminovorans HPD-2 during pyrene degradation. Transcriptomic and metabolomic analyses further revealed that co-culture significantly upregulated key pathways such as nitrogen fixation, aromatic compound degradation, protein export, and the TCA cycle in A. chroococcum HN and quorum sensing, aromatic compound degradation and ABC transporters in P. aminovorans HPD-2. Phenotypic and fluorescence in situ hybridization (FISH) assays demonstrated that A. chroococcum HN produced large amounts of biofilm and was located at the bottom of the biofilm in co-culture, whereas P. aminovorans HPD-2 attached to the surface layer and formed a bridge-like structure with A. chroococcum HN. This study demonstrates that distinct syntrophic interactions occur between A. chroococcum HN and P. aminovorans HPD-2 and provides support for their combined use in organic pollutant degradation in nitrogen-deprived environments. CI - (c) 2023. The Author(s). FAU - Wang, Xia AU - Wang X AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Teng, Ying AU - Teng Y AUID- ORCID: 0000-0003-2013-528X AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. yteng@issas.ac.cn. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. yteng@issas.ac.cn. FAU - Wang, Xiaomi AU - Wang X AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Xu, Yongfeng AU - Xu Y AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Li, Ran AU - Li R AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Sun, Yi AU - Sun Y AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Dai, Shixiang AU - Dai S AUID- ORCID: 0000-0002-6658-3785 AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Hu, Wenbo AU - Hu W AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Wang, Hongzhe AU - Wang H AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Li, Yanning AU - Li Y AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. FAU - Fang, Yan AU - Fang Y AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. AD - Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, 210008, China. FAU - Luo, Yongming AU - Luo Y AD - Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China. AD - University of the Chinese Academy of Sciences, 100049, Beijing, China. LA - eng GR - 42130718/National Natural Science Foundation of China (National Science Foundation of China)/ GR - 41991335/National Natural Science Foundation of China (National Science Foundation of China)/ PT - Journal Article DEP - 20230929 PL - England TA - ISME J JT - The ISME journal JID - 101301086 RN - N762921K75 (Nitrogen) RN - 0 (Pyrenes) RN - Azotobacter chroococcum RN - Paracoccus aminovorans SB - IM MH - *Nitrogen/metabolism MH - In Situ Hybridization, Fluorescence MH - *Nitrogen Fixation MH - Pyrenes PMC - PMC10689768 COIS- The authors declare no competing interests. EDAT- 2023/09/30 09:42 MHDA- 2023/12/04 12:43 PMCR- 2023/09/29 CRDT- 2023/09/29 23:17 PHST- 2023/07/22 00:00 [received] PHST- 2023/09/20 00:00 [accepted] PHST- 2023/09/18 00:00 [revised] PHST- 2023/12/04 12:43 [medline] PHST- 2023/09/30 09:42 [pubmed] PHST- 2023/09/29 23:17 [entrez] PHST- 2023/09/29 00:00 [pmc-release] AID - 10.1038/s41396-023-01522-w [pii] AID - 1522 [pii] AID - 10.1038/s41396-023-01522-w [doi] PST - ppublish SO - ISME J. 2023 Dec;17(12):2169-2181. doi: 10.1038/s41396-023-01522-w. Epub 2023 Sep 29.