ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae089
Shawn M Christensen, Sriram N Srinivas, Quinn S McFrederick, Bryan N Danforth, Stephen L Buchmann, Rachel L Vannette
{"title":"Symbiotic bacteria and fungi proliferate in diapause and may enhance overwintering survival in a solitary bee.","authors":"Shawn M Christensen, Sriram N Srinivas, Quinn S McFrederick, Bryan N Danforth, Stephen L Buchmann, Rachel L Vannette","doi":"10.1093/ismejo/wrae089","DOIUrl":"10.1093/ismejo/wrae089","url":null,"abstract":"<p><p>Host-microbe interactions underlie the development and fitness of many macroorganisms, including bees. Whereas many social bees benefit from vertically transmitted gut bacteria, current data suggests that solitary bees, which comprise the vast majority of species diversity within bees, lack a highly specialized gut microbiome. Here, we examine the composition and abundance of bacteria and fungi throughout the complete life cycle of the ground-nesting solitary bee Anthophora bomboides standfordiana. In contrast to expectations, immature bee stages maintain a distinct core microbiome consisting of Actinobacterial genera (Streptomyces, Nocardiodes) and the fungus Moniliella spathulata. Dormant (diapausing) larval bees hosted the most abundant and distinctive bacteria and fungi, attaining 33 and 52 times their initial copy number, respectively. We tested two adaptive hypotheses regarding microbial functions for diapausing bees. First, using isolated bacteria and fungi, we found that Streptomyces from brood cells inhibited the growth of multiple pathogenic filamentous fungi, suggesting a role in pathogen protection during overwintering, when bees face high pathogen pressure. Second, sugar alcohol composition changed in tandem with major changes in fungal abundance, suggesting links with bee cold tolerance or overwintering biology. We find that A. bomboides hosts a conserved core microbiome that may provide key fitness advantages through larval development and diapause, which raises the question of how this microbiome is maintained and faithfully transmitted between generations. Our results suggest that focus on microbiomes of mature or active insect developmental stages may overlook stage-specific symbionts and microbial fitness contributions during host dormancy.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11177884/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141065578","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Host genetic variation and specialized metabolites from wheat leaves enriches for phyllosphere Pseudomonas spp. with enriched antibiotic resistomes.","authors":"Qian Xiang, Da Lin, Zai-Jun Yang, Rui-Xia Han, Tian-Lun Zhang, Qing-Lin Chen, Dong Zhu, Josep Penuelas, Yong-Guan Zhu","doi":"10.1093/ismejo/wrae144","DOIUrl":"10.1093/ismejo/wrae144","url":null,"abstract":"<p><p>Antibiotic resistance in plant-associated microbiomes poses significant risks for agricultural ecosystems and human health. Although accumulating evidence suggests a role for plant genotypes in shaping their microbiome, almost nothing is known about how the changes of plant genetic information affect the co-evolved plant microbiome carrying antibiotic resistance genes (ARGs). Here, we selected 16 wheat cultivars and experimentally explored the impact of host genetic variation on phyllosphere microbiome, ARGs, and metabolites. Our results demonstrated that host genetic variation significantly influenced the phyllosphere resistomes. Wheat genotypes exhibiting high phyllosphere ARGs were linked to elevated Pseudomonas populations, along with increased abundances of Pseudomonas aeruginosa biofilm formation genes. Further analysis of 350 Pseudomonas spp. genomes from diverse habitats at a global scale revealed that nearly all strains possess multiple ARGs, virulence factor genes (VFGs), and mobile genetic elements (MGEs) on their genomes, albeit with lower nucleotide diversity compared to other species. These findings suggested that the proliferation of Pseudomonas spp. in the phyllosphere significantly contributed to antibiotic resistance. We further observed direct links between the upregulated leaf metabolite DIMBOA-Glc, Pseudomonas spp., and enrichment of phyllosphere ARGs, which were corroborated by microcosm experiments demonstrating that DIMBOA-Glc significantly enhanced the relative abundance of Pseudomonas spp. Overall, alterations in leaf metabolites resulting from genetic variation throughout plant evolution may drive the development of highly specialized microbial communities capable of enriching phyllosphere ARGs. This study enhances our understanding of how plants actively shape microbial communities and clarifies the impact of host genetic variation on the plant resistomes.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11334211/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141793968","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae159
Chyrene Moncada, Carol Arnosti, Jan D Brüwer, Dirk de Beer, Rudolf Amann, Katrin Knittel
{"title":"Niche separation in bacterial communities and activities in porewater, loosely attached, and firmly attached fractions in permeable surface sediments.","authors":"Chyrene Moncada, Carol Arnosti, Jan D Brüwer, Dirk de Beer, Rudolf Amann, Katrin Knittel","doi":"10.1093/ismejo/wrae159","DOIUrl":"10.1093/ismejo/wrae159","url":null,"abstract":"<p><p>Heterotrophic microbes are central to organic matter degradation and transformation in marine sediments. Currently, most investigations of benthic microbiomes do not differentiate between processes in the porewater and on the grains and, hence, only show a generalized picture of the community. This limits our understanding of the structure and functions of sediment microbiomes. To address this problem, we fractionated sandy surface sediment microbial communities from a coastal site in Isfjorden, Svalbard, into cells associated with the porewater, loosely attached to grains, and firmly attached to grains; we found dissimilar bacterial communities and metabolic activities in these fractions. Most (84%-89%) of the cells were firmly attached, and this fraction comprised more anaerobes, such as sulfate reducers, than the other fractions. The porewater and loosely attached fractions (3% and 8%-13% of cells, respectively) had more aerobic heterotrophs. These two fractions generally showed a higher frequency of dividing cells, polysaccharide (laminarin) hydrolysis rates, and per-cell O2 consumption than the firmly attached cells. Thus, the different fractions occupy distinct niches within surface sediments: the firmly attached fraction is potentially made of cells colonizing areas on the grain that are protected from abrasion, but might be more diffusion-limited for organic matter and electron acceptors. In contrast, the porewater and loosely attached fractions are less resource-limited and have faster growth. Their cell numbers are kept low possibly through abrasion and exposure to grazers. Differences in community composition and activity of these cell fractions point to their distinct roles and contributions to carbon cycling within surface sediments.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11368169/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141903449","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Role of Type VI secretion system in pathogenic remodeling of host gut microbiota during Aeromonas veronii infection.","authors":"Xiaoli Jiang, Hanzeng Li, Jiayue Ma, Hong Li, Xiang Ma, Yanqiong Tang, Juanjuan Li, Xue Chi, Yong Deng, Sheng Zeng, Zhu Liu","doi":"10.1093/ismejo/wrae053","DOIUrl":"10.1093/ismejo/wrae053","url":null,"abstract":"<p><p>Intestinal microbial disturbance is a direct cause of host disease. The bacterial Type VI secretion system (T6SS) often plays a crucial role in the fitness of pathogenic bacteria by delivering toxic effectors into target cells. However, its impact on the gut microbiota and host pathogenesis is poorly understood. To address this question, we characterized a new T6SS in the pathogenic Aeromonas veronii C4. First, we validated the secretion function of the core machinery of A. veronii C4 T6SS. Second, we found that the pathogenesis and colonization of A. veronii C4 is largely dependent on its T6SS. The effector secretion activity of A. veronii C4 T6SS not only provides an advantage in competition among bacteria in vitro, but also contributes to occupation of an ecological niche in the nutritionally deficient and anaerobic environment of the host intestine. Metagenomic analysis showed that the T6SS directly inhibits or eliminates symbiotic strains from the intestine, resulting in dysregulated gut microbiome homeostasis. In addition, we identified three unknown effectors, Tse1, Tse2, and Tse3, in the T6SS, which contribute to T6SS-mediated bacterial competition and pathogenesis by impairing targeted cell integrity. Our findings highlight that T6SS can remodel the host gut microbiota by intricate interplay between T6SS-mediated bacterial competition and altered host immune responses, which synergistically promote pathogenesis of A. veronii C4. Therefore, this newly characterized T6SS could represent a general interaction mechanism between the host and pathogen, and may offer a potential therapeutic target for controlling bacterial pathogens.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11014884/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140295078","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Gut microbiota facilitate adaptation of invasive moths to new host plants.","authors":"Shouke Zhang, Feng Song, Jie Wang, Xiayu Li, Yuxin Zhang, Wenwu Zhou, Letian Xu","doi":"10.1093/ismejo/wrae031","DOIUrl":"10.1093/ismejo/wrae031","url":null,"abstract":"<p><p>Gut microbiota are important in the adaptation of phytophagous insects to their plant hosts. However, the interaction between gut microbiomes and pioneering populations of invasive insects during their adaptation to new hosts, particularly in the initial phases of invasion, has been less studied. We studied the contribution of the gut microbiome to host adaptation in the globally recognized invasive pest, Hyphantria cunea, as it expands its range into southern China. The southern population of H. cunea shows effective adaptation to Metasequoia glyptostroboides and exhibits greater larval survival on Metasequoia than the original population. Genome resequencing revealed no significant differences in functions related to host adaptation between the two populations. The compatibility between southern H. cunea populations and M. glyptostroboides revealed a correlation between the abundance of several gut bacteria genera (Bacteroides, Blautia, and Coprococcus) and H. cunea survival. Transplanting the larval gut microbiome from southern to northern populations enhanced the adaptability of the latter to the previously unsuitable plant M. glyptostroboides. This research provides evidence that the gut microbiome of pioneering populations can enhance the compatibility of invasive pests to new hosts and enable more rapid adaptation to new habitats.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":11.0,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10980833/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139998136","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae082
Wei Li, David Baliu-Rodriguez, Sanduni H Premathilaka, Sharmila I Thenuwara, Jeffrey A Kimbrel, Ty J Samo, Christina Ramon, Erik Anders Kiledal, Sara R Rivera, Jenan Kharbush, Dragan Isailovic, Peter K Weber, Gregory J Dick, Xavier Mayali
{"title":"Microbiome processing of organic nitrogen input supports growth and cyanotoxin production of Microcystis aeruginosa cultures.","authors":"Wei Li, David Baliu-Rodriguez, Sanduni H Premathilaka, Sharmila I Thenuwara, Jeffrey A Kimbrel, Ty J Samo, Christina Ramon, Erik Anders Kiledal, Sara R Rivera, Jenan Kharbush, Dragan Isailovic, Peter K Weber, Gregory J Dick, Xavier Mayali","doi":"10.1093/ismejo/wrae082","DOIUrl":"10.1093/ismejo/wrae082","url":null,"abstract":"<p><p>Nutrient-induced blooms of the globally abundant freshwater toxic cyanobacterium Microcystis cause worldwide public and ecosystem health concerns. The response of Microcystis growth and toxin production to new and recycled nitrogen (N) inputs and the impact of heterotrophic bacteria in the Microcystis phycosphere on these processes are not well understood. Here, using microbiome transplant experiments, cyanotoxin analysis, and nanometer-scale stable isotope probing to measure N incorporation and exchange at single cell resolution, we monitored the growth, cyanotoxin production, and microbiome community structure of several Microcystis strains grown on amino acids or proteins as the sole N source. We demonstrate that the type of organic N available shaped the microbial community associated with Microcystis, and external organic N input led to decreased bacterial colonization of Microcystis colonies. Our data also suggest that certain Microcystis strains could directly uptake amino acids, but with lower rates than heterotrophic bacteria. Toxin analysis showed that biomass-specific microcystin production was not impacted by N source (i.e. nitrate, amino acids, or protein) but rather by total N availability. Single-cell isotope incorporation revealed that some bacterial communities competed with Microcystis for organic N, but other communities promoted increased N uptake by Microcystis, likely through ammonification or organic N modification. Our laboratory culture data suggest that organic N input could support Microcystis blooms and toxin production in nature, and Microcystis-associated microbial communities likely play critical roles in this process by influencing cyanobacterial succession through either decreasing (via competition) or increasing (via biotransformation) N availability, especially under inorganic N scarcity.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11126159/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140892844","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae116
Nina Roothans, Minke Gabriëls, Thomas Abeel, Martin Pabst, Mark C M van Loosdrecht, Michele Laureni
{"title":"Aerobic denitrification as an N2O source from microbial communities.","authors":"Nina Roothans, Minke Gabriëls, Thomas Abeel, Martin Pabst, Mark C M van Loosdrecht, Michele Laureni","doi":"10.1093/ismejo/wrae116","DOIUrl":"10.1093/ismejo/wrae116","url":null,"abstract":"<p><p>Nitrous oxide (N2O) is a potent greenhouse gas of primarily microbial origin. Oxic and anoxic emissions are commonly ascribed to autotrophic nitrification and heterotrophic denitrification, respectively. Beyond this established dichotomy, we quantitatively show that heterotrophic denitrification can significantly contribute to aerobic nitrogen turnover and N2O emissions in complex microbiomes exposed to frequent oxic/anoxic transitions. Two planktonic, nitrification-inhibited enrichment cultures were established under continuous organic carbon and nitrate feeding, and cyclic oxygen availability. Over a third of the influent organic substrate was respired with nitrate as electron acceptor at high oxygen concentrations (>6.5 mg/L). N2O accounted for up to one-quarter of the nitrate reduced under oxic conditions. The enriched microorganisms maintained a constitutive abundance of denitrifying enzymes due to the oxic/anoxic frequencies exceeding their protein turnover-a common scenario in natural and engineered ecosystems. The aerobic denitrification rates are ascribed primarily to the residual activity of anaerobically synthesised enzymes. From an ecological perspective, the selection of organisms capable of sustaining significant denitrifying activity during aeration shows their competitive advantage over other heterotrophs under varying oxygen availabilities. Ultimately, we propose that the contribution of heterotrophic denitrification to aerobic nitrogen turnover and N2O emissions is currently underestimated in dynamic environments.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11272060/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141447411","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Chemolithoautotrophic diazotrophs dominate dark nitrogen fixation in mangrove sediments.","authors":"Shasha Wang, Lijing Jiang, Zhuoming Zhao, Zhen Chen, Jun Wang, Karine Alain, Liang Cui, Yangsheng Zhong, Yongyi Peng, Qiliang Lai, Xiyang Dong, Zongze Shao","doi":"10.1093/ismejo/wrae119","DOIUrl":"10.1093/ismejo/wrae119","url":null,"abstract":"<p><p>Diazotrophic microorganisms regulate marine productivity by alleviating nitrogen limitation. So far chemolithoautotrophic bacteria are widely recognized as the principal diazotrophs in oligotrophic marine and terrestrial ecosystems. However, the contribution of chemolithoautotrophs to nitrogen fixation in organic-rich habitats remains unclear. Here, we utilized metagenomic and metatranscriptomic approaches integrated with cultivation assays to investigate the diversity, distribution, and activity of diazotrophs residing in Zhangzhou mangrove sediments. Physicochemical assays show that the studied mangrove sediments are typical carbon-rich, sulfur-rich, nitrogen-limited, and low-redox marine ecosystems. These sediments host a wide phylogenetic variety of nitrogenase genes, including groups I-III and VII-VIII. Unexpectedly diverse chemolithoautotrophic taxa including Campylobacteria, Gammaproteobacteria, Zetaproteobacteria, and Thermodesulfovibrionia are the predominant and active nitrogen fixers in the 0-18 cm sediment layer. In contrast, the 18-20 cm layer is dominated by active diazotrophs from the chemolithoautotrophic taxa Desulfobacterota and Halobacteriota. Further analysis of MAGs shows that the main chemolithoautotrophs can fix nitrogen by coupling the oxidation of hydrogen, reduced sulfur, and iron, with the reduction of oxygen, nitrate, and sulfur. Culture experiments further demonstrate that members of chemolithoautotrophic Campylobacteria have the nitrogen-fixing capacity driven by hydrogen and sulfur oxidation. Activity measurements confirm that the diazotrophs inhabiting mangrove sediments preferentially drain energy from diverse reduced inorganic compounds other than from organics. Overall, our results suggest that chemolithoautotrophs rather than heterotrophs are dominant nitrogen fixers in mangrove sediments. This study underscores the significance of chemolithoautotrophs in carbon-dominant ecosystems.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11474244/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141447413","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae118
Yin Ye, Lu Zhang, Xiaohui Hong, Man Chen, Xing Liu, Shungui Zhou
{"title":"Interspecies ecological competition rejuvenates decayed Geobacter electroactive biofilm.","authors":"Yin Ye, Lu Zhang, Xiaohui Hong, Man Chen, Xing Liu, Shungui Zhou","doi":"10.1093/ismejo/wrae118","DOIUrl":"10.1093/ismejo/wrae118","url":null,"abstract":"<p><p>Bioelectrochemical systems (BESs) exploit electroactive biofilms (EABs) for promising applications in biosensing, wastewater treatment, energy production, and chemical biosynthesis. However, during the operation of BESs, EABs inevitably decay. Seeking approaches to rejuvenate decayed EABs is critical for the sustainability and practical application of BESs. Prophage induction has been recognized as the primary reason for EAB decay. Herein, we report that introducing a competitive species of Geobacter uraniireducens suspended prophage induction in Geobacter sulfurreducens and thereby rejuvenated the decayed G. sulfurreducens EAB. The transcriptomic profile of G. sulfurreducens demonstrated that the addition of G. uraniireducens significantly affected the expression of metabolism- and stress response system-related genes and in particular suppressed the induction of phage-related genes. Mechanistic analyses revealed that interspecies ecological competition exerted by G. uraniireducens suppressed prophage induction. Our findings not only reveal a novel strategy to rejuvenate decayed EABs, which is significant for the sustainability of BESs, but also provide new knowledge for understanding phage-host interactions from an ecological perspective, with implications for developing therapies to defend against phage attack.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11227281/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141447414","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2024-01-08DOI: 10.1093/ismejo/wrae120
Sang-Moo Lee, Roniya Thapa Magar, Min Kyeong Jung, Hyun Gi Kong, Ju Yeon Song, Joo Hwan Kwon, Minseo Choi, Hyoung Ju Lee, Seung Yeup Lee, Raees Khan, Jihyun F Kim, Seon-Woo Lee
{"title":"Rhizobacterial syntrophy between a helper and a beneficiary promotes tomato plant health.","authors":"Sang-Moo Lee, Roniya Thapa Magar, Min Kyeong Jung, Hyun Gi Kong, Ju Yeon Song, Joo Hwan Kwon, Minseo Choi, Hyoung Ju Lee, Seung Yeup Lee, Raees Khan, Jihyun F Kim, Seon-Woo Lee","doi":"10.1093/ismejo/wrae120","DOIUrl":"10.1093/ismejo/wrae120","url":null,"abstract":"<p><p>Microbial interactions impact the functioning of microbial communities. However, microbial interactions within host-associated communities remain poorly understood. Here, we report that the beneficiary rhizobacterium Niallia sp. RD1 requires the helper Pseudomonas putida H3 for bacterial growth and beneficial interactions with the plant host. In the absence of the helper H3 strain, the Niallia sp. RD1 strain exhibited weak respiration and elongated cell morphology without forming bacterial colonies. A transposon mutant of H3 in a gene encoding succinate-semialdehyde dehydrogenase displayed much attenuated support of RD1 colony formation. Through the subsequent addition of succinate to the media, we found that succinate serves as a public good that supports RD1 growth. Comparative genome analysis highlighted that RD1 lacked the gene for sufficient succinate, suggesting its evolution as a beneficiary of succinate biosynthesis. The syntrophic interaction between RD1 and H3 efficiently protected tomato plants from bacterial wilt and promoted tomato growth. The addition of succinate to the medium restored complex II-dependent respiration in RD1 and facilitated the cultivation of various bacterial isolates from the rhizosphere. Taken together, we delineate energy auxotrophic beneficiaries ubiquitous in the microbial community, and these beneficiaries could benefit host plants with the aid of helpers in the rhizosphere.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.8,"publicationDate":"2024-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11253211/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141477901","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}