The ISME Journal最新文献

Chronic exposure to polycyclic aromatic hydrocarbons alters skin virome composition and virus–host interactions 长期接触多环芳烃会改变皮肤病毒组的组成和病毒与宿主的相互作用

The ISME Journal Pub Date : 2024-10-25 DOI: 10.1093/ismejo/wrae218

Shicong Du, Xinzhao Tong, Marcus H Y Leung, Richard J Betts, Anthony C Woo, Philippe Bastien, Namita Misra, Luc Aguilar, Cécile Clavaud, Patrick K H Lee

{"title":"Chronic exposure to polycyclic aromatic hydrocarbons alters skin virome composition and virus–host interactions","authors":"Shicong Du, Xinzhao Tong, Marcus H Y Leung, Richard J Betts, Anthony C Woo, Philippe Bastien, Namita Misra, Luc Aguilar, Cécile Clavaud, Patrick K H Lee","doi":"10.1093/ismejo/wrae218","DOIUrl":"https://doi.org/10.1093/ismejo/wrae218","url":null,"abstract":"Exposure to polycyclic aromatic hydrocarbons (PAHs) in polluted air influences the composition of the skin microbiome, which in turn is associated with altered skin phenotypes. However, the interactions between PAH exposure and viromes are unclear. This study aims to elucidate how PAH exposure affects the composition and function of skin viruses, their role in shaping the metabolism of bacterial hosts, and the subsequent effects on skin phenotype. We analyzed metagenomes from cheek skin swabs collected from 124 Chinese women in our previous study and found that the viruses associated with the two microbiome cutotypes had distinct diversities, compositions, functions, and lifestyles following PAH exposure. Moreover, exposure to high concentrations of PAHs substantially increased interactions between viruses and certain biodegrading bacteria. Under high-PAH exposure, the viruses were enriched in xenobiotic degradation functions, and there was evidence suggesting that the insertion of bacteriophage-encoded auxiliary metabolic genes into hosts aids biodegradation. Under low-PAH exposure conditions, the interactions followed the “Piggyback-the-Winner” model, with Cutibacterium acnes being “winners,” whereas under high-PAH exposure, they followed the “Piggyback-the-Persistent” model, with biodegradation bacteria being “persistent.” These findings highlight the impact of air pollutants on skin bacteria and viruses, their interactions, and their modulation of skin health. Understanding these intricate relationships could provide insights for developing targeted strategies to maintain skin health in polluted environments, emphasizing the importance of mitigating pollutant exposure and harnessing the potential of viruses to help counteract the adverse effects.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142490401","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0

Metagenomic time-series reveals a western English Channel viral community dominated by members with strong seasonal signals 元基因组时间序列显示英吉利海峡西部病毒群落以具有强烈季节性信号的成员为主

The ISME Journal Pub Date : 2024-10-23 DOI: 10.1093/ismejo/wrae216

Luis M Bolaños, Michelle Michelsen, Ben Temperton

{"title":"Metagenomic time-series reveals a western English Channel viral community dominated by members with strong seasonal signals","authors":"Luis M Bolaños, Michelle Michelsen, Ben Temperton","doi":"10.1093/ismejo/wrae216","DOIUrl":"https://doi.org/10.1093/ismejo/wrae216","url":null,"abstract":"Marine viruses are key players of ocean biogeochemistry, profoundly influencing microbial community ecology and evolution. Despite their importance, few studies have explored continuous inter-seasonal viral metagenomic time-series in marine environments. Viral dynamics are complex, influenced by multiple factors such as host population dynamics and environmental conditions. To disentangle the complexity of viral communities, we developed an unsupervised machine learning framework to classify viral contigs into \"chronotypes\" based on temporal abundance patterns. Analysing an inter-seasonal monthly time-series of surface viral metagenomes from the Western English Channel, we identified chronotypes and compared their functional and evolutionary profiles. Results revealed a consistent annual cycle with steep compositional changes from winter to summer and steadier transitions from summer to winter. Seasonal chronotypes were enriched in potential auxiliary metabolic genes of the ferrochelatases and 2OG-Fe(II) oxygenase orthologous groups compared to non-seasonal types. Chronotypes clustered into four groups based on their correlation profiles with environmental parameters, primarily driven by temperature and nutrients. Viral contigs exhibited a rapid turnover of polymorphisms, akin to Red Queen dynamics. However, within seasonal chronotypes, some sequences exhibited annual polymorphism recurrence, suggesting that a fraction of the seasonal viral populations evolve more slowly. Classification into chronotypes revealed viral genomic signatures linked to temporal patterns, likely reflecting metabolic adaptations to environmental fluctuations and host dynamics. This novel framework enables the identification of long-term trends in viral composition, environmental influences on genomic structure, and potential viral interactions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488821","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0

Ecological success of extreme halophiles subjected to recurrent osmotic disturbances is primarily driven by congeneric species replacement 受到经常性渗透干扰的极端嗜卤生物的生态成功主要是由同源物种替换驱动的

The ISME Journal Pub Date : 2024-10-23 DOI: 10.1093/ismejo/wrae215

Esteban Bustos-Caparros, Tomeu Viver, Juan F Gago, Luis Miguel Rodriguez-Rojas, Janet K Hatt, Stephanus N Venter, Bernhard M Fuchs, Rudolf Amann, Rafael Bosch, Konstantinos T Konstantinidis, Ramon Rossello-Mora

{"title":"Ecological success of extreme halophiles subjected to recurrent osmotic disturbances is primarily driven by congeneric species replacement","authors":"Esteban Bustos-Caparros, Tomeu Viver, Juan F Gago, Luis Miguel Rodriguez-Rojas, Janet K Hatt, Stephanus N Venter, Bernhard M Fuchs, Rudolf Amann, Rafael Bosch, Konstantinos T Konstantinidis, Ramon Rossello-Mora","doi":"10.1093/ismejo/wrae215","DOIUrl":"https://doi.org/10.1093/ismejo/wrae215","url":null,"abstract":"To understand how extreme halophiles respond to recurrent disturbances, we challenged the communities thriving in salt-saturated (~36% salts) ~230 L brine mesocosms to repeated dilutions down to 13% (D13 mesocosm) or 20% (D20 mesocosm) salts each time mesocosms reached salt saturation due to evaporation (for 10 and 17 cycles, respectively) over 813 days. Depending on the magnitude of dilution, the most prevalent species, Haloquadratum walsbyi and Salinibacter ruber, either increased in dominance by replacing less competitive populations (for D20, moderate stress conditions), or severely decreased in abundance and were eventually replaced by other congeneric species better adapted to the higher osmotic stress (for D13, strong stress conditions). Congeneric species replacement was commonly observed within additional abundant genera in response to changes in environmental or biological conditions (e.g. phage predation) within the same system and under a controlled perturbation of a relevant environmental parameter. Therefore, a genus is an ecologically important level of diversity organization, not just a taxonomic rank, that persists in the environment based on congeneric species replacement due to relatively high functional overlap (gene sharing), with important consequences for the success of the lineage, and similar to the success of a species via strain-replacement. Further, our results showed that successful species were typically accompanied by the emergence of their own viral cohorts, whose intra-cohort diversity appeared to strongly covary with, and likely drive, the intra-host diversity. Collectively, our results show that brine communities are ecologically resilient and continuously adapting to changing environments by transitioning to alternative stable states.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488822","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0

Repeated horizontal acquisition of lagriamide-producing symbionts in Lagriinae beetles 拉格瑞纳甲虫重复水平获取拉格瑞纳共生体

The ISME Journal Pub Date : 2024-10-23 DOI: 10.1093/ismejo/wrae211

Siddharth Uppal, Samantha C Waterworth, Alina Nick, Heiko Vogel, Laura V Flórez, Martin Kaltenpoth, Jason C Kwan

{"title":"Repeated horizontal acquisition of lagriamide-producing symbionts in Lagriinae beetles","authors":"Siddharth Uppal, Samantha C Waterworth, Alina Nick, Heiko Vogel, Laura V Flórez, Martin Kaltenpoth, Jason C Kwan","doi":"10.1093/ismejo/wrae211","DOIUrl":"https://doi.org/10.1093/ismejo/wrae211","url":null,"abstract":"Microbial symbionts associate with multicellular organisms on a continuum from facultative associations to mutual codependency. In the oldest intracellular symbioses there is exclusive vertical symbiont transmission, and co-diversification of symbiotic partners over millions of years. Such symbionts often undergo genome reduction due to low effective population sizes, frequent population bottlenecks, and reduced purifying selection. Here, we describe multiple independent acquisition events of closely related defensive symbionts followed by genome erosion in a group of Lagriinae beetles. Previous work in Lagria villosa revealed the dominant genome-eroded symbiont of the genus Burkholderia produces the antifungal compound lagriamide, protecting the beetle’s eggs and larvae from antagonistic fungi. Here, we use metagenomics to assemble 11 additional genomes of lagriamide-producing symbionts from seven different host species within Lagriinae from five countries, to unravel the evolutionary history of this symbiotic relationship. In each host, we detected one dominant genome-eroded Burkholderia symbiont encoding the lagriamide biosynthetic gene cluster. However, we did not find evidence for host-symbiont co-diversification, or for monophyly of the lagriamide-producing symbionts. Instead, our analyses support a single ancestral acquisition of the gene cluster followed by at least four independent symbiont acquisitions and subsequent genome erosion in each lineage. By contrast, a clade of plant-associated relatives retained large genomes but secondarily lost the lagriamide gene cluster. Our results, therefore, reveal a dynamic evolutionary history with multiple independent symbiont acquisitions characterized by a high degree of specificity, and highlight the importance of the specialized metabolite lagriamide for the establishment and maintenance of this defensive symbiosis.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488817","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0

Trade-offs between receptor modification and fitness drive host-bacteriophage co-evolution leading to phage extinction or co-existence 受体修饰和适应性之间的权衡推动宿主-噬菌体共同进化，导致噬菌体灭绝或共存

The ISME Journal Pub Date : 2024-10-23 DOI: 10.1093/ismejo/wrae214

Lin Chen, Xue Zhao, Shelyn Wongso, Zhuohui Lin, Siyun Wang

{"title":"Trade-offs between receptor modification and fitness drive host-bacteriophage co-evolution leading to phage extinction or co-existence","authors":"Lin Chen, Xue Zhao, Shelyn Wongso, Zhuohui Lin, Siyun Wang","doi":"10.1093/ismejo/wrae214","DOIUrl":"https://doi.org/10.1093/ismejo/wrae214","url":null,"abstract":"Parasite–host co-evolution results in population extinction or co-existence, yet the factors driving these distinct outcomes remain elusive. In this study, Salmonella strains were individually co-evolved with the lytic phage SF1 for 30 days, resulting in phage extinction or co-existence. We conducted a systematic investigation into the phenotypic and genetic dynamics of evolved host cells and phages to elucidate the evolutionary mechanisms. Throughout co-evolution, host cells displayed diverse phage resistance patterns: sensitivity, partial resistance, and complete resistance, to wild-type phage. Moreover, phage resistance strength showed a robust linear correlation with phage adsorption, suggesting that surface modification-mediated phage attachment predominates as the resistance mechanism in evolved bacterial populations. Additionally, bacterial isolates eliminating phages exhibited higher mutation rates and lower fitness costs in developing resistance compared to those leading to co-existence. Phage resistance genes were classified into two categories: key mutations, characterized by nonsense/frameshift mutations in rfaH-regulated rfb genes, leading to the removal of the receptor O-antigen; and secondary mutations, which involve less critical modifications, such as fimbrial synthesis and tRNA modification. The accumulation of secondary mutations resulted in partial and complete resistance, which could be overcome by evolved phages, whereas key mutations conferred undefeatable complete resistance by deleting receptors. In conclusion, higher key mutation frequencies with lower fitness costs promised strong resistance and eventual phage extinction, whereas deficiencies in fitness cost, mutation rate, and key mutation led to co-existence. Our findings reveal the distinct population dynamics and evolutionary trade-offs of phage resistance during co-evolution, thereby deepening our understanding of microbial interactions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488818","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0

Taeniasis impacts human gut microbiome composition and function 泰纳丝虫病影响人类肠道微生物组的组成和功能

The ISME Journal Pub Date : 2024-10-23 DOI: 10.1093/ismejo/wrae213

Wenjie Mu, Pingping Ma, Yugui Wang, Yaqi Li, Yingying Ding, Yang Zou, Lixia Pu, Qi Yan, Haoyue Kong, Xiaola Guo, Aijiang Guo, Hailong Li, Shuai Wang

{"title":"Taeniasis impacts human gut microbiome composition and function","authors":"Wenjie Mu, Pingping Ma, Yugui Wang, Yaqi Li, Yingying Ding, Yang Zou, Lixia Pu, Qi Yan, Haoyue Kong, Xiaola Guo, Aijiang Guo, Hailong Li, Shuai Wang","doi":"10.1093/ismejo/wrae213","DOIUrl":"https://doi.org/10.1093/ismejo/wrae213","url":null,"abstract":"Human taeniasis, caused by Taenia tapeworms, is a global parasitic disease with significant implications for public health and food safety. These tapeworms can grow to considerable sizes and potentially impact the microecology of the host gut. Despite their importance, the effects of Taenia infection on host gut microbiota haven’t been thoroughly investigated. In this study, we conducted a cross-sectional analysis of the gut microbiome in patients infected with Taenia asiatica (n = 87) compared to healthy controls (n = 79) in the Dali cohort, China. We also performed a longitudinal assessment of microbial changes following deworming in a subset of patients (n = 24). Our findings reveal a significant shift in gut microbial composition, characterized by increased alpha-diversity and an enrichment of Prevotella-driven enterotypes in infected patients compared to healthy controls. The stability of these microbial features post-deworming varied widely among individuals and was lower in those with lower initial alpha diversity and Prevotella-enterotype before deworming. We observed a significant depletion of Bifidobacterium species in infected individuals, regardless of enterotypes, and these prebiotics did not recover post-deworming. Metabolic network analysis and in vitro experiments suggest that the reduction of Bifidobacterium was linked to metabolic competition for ecological niches or nutrients, particularly stachyose, from other microbes rather than the parasitism itself. Furthermore, our machine learning analysis demonstrated that taxa associated with Bifidobacterium in stachyose metabolism could robustly predict infection but could not predict deworming. This study highlights the substantial impact of taeniasis on the human gut microbiome and overall gut health.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142488823","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0

Marine N2-fixer Crocosphaera waterburyi 海洋固氮动物 Crocosphaera waterburyi

The ISME Journal Pub Date : 2024-10-23 DOI: 10.1093/ismejo/wrae217

Catie S Cleveland, Kendra A Turk-Kubo, Yiming Zhao, Jonathan P Zehr, Eric A Webb

引用次数: 0

Rhizobacterial syntrophy between a helper and a beneficiary promotes tomato plant health 帮助者和受益者之间的根瘤菌合成作用促进番茄植株健康

The ISME Journal Pub Date : 2024-10-22 DOI: 10.1093/ismejo/wrae210

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/wrae210","DOIUrl":"https://doi.org/10.1093/ismejo/wrae210","url":null,"abstract":"None declared.Conflicts of interestMicrobial interactions impact the functioning of microbial communities. However, microbial interactions within host-associated communities remains 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 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 the 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.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142487603","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0

Prophages in Vibrio 弧菌中的噬菌体

The ISME Journal Pub Date : 2024-10-17 DOI: 10.1093/ismejo/wrae202

Kerrin Steensen, Joana Séneca, Nina Bartlau, Xiaoqian A Yu, Fatima A Hussain, Martin F Polz

{"title":"Prophages in Vibrio","authors":"Kerrin Steensen, Joana Séneca, Nina Bartlau, Xiaoqian A Yu, Fatima A Hussain, Martin F Polz","doi":"10.1093/ismejo/wrae202","DOIUrl":"https://doi.org/10.1093/ismejo/wrae202","url":null,"abstract":"Although tailed bacteriophages (phages) of the class Caudoviricetes are thought to constitute the most abundant and ecologically relevant group of phages that can integrate their genome into the host chromosome, it is becoming increasingly clear that other prophages are widespread. Here, we show that prophages derived from filamentous and tailless phages with genome sizes below 16 kb make up the majority of prophages in marine bacteria of the genus Vibrio. To estimate prophage prevalence unaffected by database biases, we combined comparative genomics and chemical induction of 58 diverse Vibrio cyclitrophicus isolates, resulting in 107 well-curated prophages. Complemented with computationally predicted prophages, we obtained 1,158 prophages from 931 naturally co-existing strains of the family Vibrionaceae. Prophages resembling tailless and filamentous phages predominated, accounting for 80% of all prophages in V. cyclitrophicus and 60% across the Vibrionaceae. In our experimental model, prophages of all three viral realms actively replicated upon induction indicating their ability to transfer to new hosts. Indeed, prophages were rapidly gained and lost, as suggested by variable prophage content between closely related V. cyclitrophicus. Prophages related to filamentous and tailless phages were integrated into only three genomic locations and restored the function of their integration site. Despite their small size, they contained highly diverse accessory genes that may contribute to host fitness, such as phage defense systems. We propose that, like their well-studied tailed equivalent, tailless and filamentous temperate phages are active and highly abundant drivers of host ecology and evolution in marine Vibrio, which have been largely overlooked.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142449618","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0

Resource sharing of an infant gut microbiota synthetic community in combinations of human milk oligosaccharides 母乳低聚糖组合中婴儿肠道微生物群合成群落的资源共享

The ISME Journal Pub Date : 2024-10-17 DOI: 10.1093/ismejo/wrae209

Athanasia Ioannou, Maryse D Berkhout, William T Scott, Bernadet Blijenberg, Sjef Boeren, Marko Mank, Jan Knol, Clara Belzer

{"title":"Resource sharing of an infant gut microbiota synthetic community in combinations of human milk oligosaccharides","authors":"Athanasia Ioannou, Maryse D Berkhout, William T Scott, Bernadet Blijenberg, Sjef Boeren, Marko Mank, Jan Knol, Clara Belzer","doi":"10.1093/ismejo/wrae209","DOIUrl":"https://doi.org/10.1093/ismejo/wrae209","url":null,"abstract":"Quickly after birth, the gut microbiota is shaped via species acquisition and resource pressure. Breastmilk, and more specifically, human milk oligosaccharides are a determining factor in the formation of microbial communities and the interactions between bacteria. Prominent human milk oligosaccharide degraders have been rigorously characterized, but it is not known how the gut microbiota is shaped as a complex community. Here, we designed BIG-Syc, a synthetic community of 13 strains from the gut of vaginally born, breastfed infants. BIG-Syc replicated key compositional, metabolic, and proteomic characteristics of the gut microbiota of infants. Upon fermentation of a 4 and 5 human milk oligosaccharide mix, BIG-Syc demonstrated different compositional and proteomic profiles, with Bifidobacterium infantis and Bifidobacterium bifidum suppressing one another. The mix of 5 human milk oligosaccharides resulted in a more diverse composition with dominance of B. bifidum, whereas that with 4 human milk oligosaccharides supported the dominance of B. infantis, in 4 of 6 replicates. Reintroduction of bifidobacteria to BIG-Syc led to their engraftment and establishment of their niche. Based on proteomics and genome-scale metabolic models, we reconstructed the carbon source utilization and metabolite and gas production per strain. BIG-Syc demonstrated teamwork as cross-feeders utilized simpler carbohydrates, organic acids, and gases released from human milk oligosaccharide degraders. Collectively, our results showed that human milk oligosaccharides prompt resource-sharing for their complete degradation while leading to a different compositional and functional profile in the community. At the same time, BIG-Syc proved to be an accurate model for the representation of intra-microbe interactions.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142449619","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

引用次数: 0