Mengxiong Wu, Xiawei Liu, J Pamela Engelberts, Gene W Tyson, Simon J McIlroy, Jianhua Guo
The bacterial species ‘Candidatus Alkanivorans nitratireducens’ was recently demonstrated to mediate nitrate-dependent anaerobic oxidation of short-chain gaseous alkanes (SCGAs). In previous bioreactor enrichment studies1,2, the species appeared to reduce nitrate in two phases, switching from denitrification to dissimilatory nitrate reduction to ammonium (DNRA) in response to nitrite accumulation. The regulation of this switch or the nature of potential syntrophic partnerships with other microorganisms remains unclear. Here, we describe anaerobic multispecies cultures of bacteria which couple the oxidation of propane and butane to nitrate reduction and the oxidation of ammonium (anammox). Batch tests with 15N-isotope labelling and multi-omic analyses collectively supported a syntrophic partnership between ‘Ca. A. nitratireducens’ and anammox bacteria, with the former species mediating nitrate-driven oxidation of SCGAs, supplying the latter with nitrite for the oxidation of ammonium. The elimination of nitrite accumulation by the anammox substantially increased SCGA and nitrate consumption rates, whereas suppressing DNRA. Removing ammonium supply led to its eventual production, the accumulation of nitrite, and the upregulation of DNRA gene expression for the abundant ‘Ca. A. nitratireducens’. Increasing the supply of SCGA had a similar effect in promoting DNRA. Our results suggest that ‘Ca. A. nitratireducens’ switches to DNRA to alleviate oxidative stress caused by nitrite accumulation, giving further insight into adaptability and ecology of this microorganism. Our findings also have important implications for the understanding of the fate of nitrogen and SCGAs in anaerobic environments.
{"title":"Anaerobic oxidation of ammonium and short-chain gaseous alkanes coupled to nitrate reduction by a bacterial consortium","authors":"Mengxiong Wu, Xiawei Liu, J Pamela Engelberts, Gene W Tyson, Simon J McIlroy, Jianhua Guo","doi":"10.1093/ismejo/wrae063","DOIUrl":"https://doi.org/10.1093/ismejo/wrae063","url":null,"abstract":"The bacterial species ‘Candidatus Alkanivorans nitratireducens’ was recently demonstrated to mediate nitrate-dependent anaerobic oxidation of short-chain gaseous alkanes (SCGAs). In previous bioreactor enrichment studies1,2, the species appeared to reduce nitrate in two phases, switching from denitrification to dissimilatory nitrate reduction to ammonium (DNRA) in response to nitrite accumulation. The regulation of this switch or the nature of potential syntrophic partnerships with other microorganisms remains unclear. Here, we describe anaerobic multispecies cultures of bacteria which couple the oxidation of propane and butane to nitrate reduction and the oxidation of ammonium (anammox). Batch tests with 15N-isotope labelling and multi-omic analyses collectively supported a syntrophic partnership between ‘Ca. A. nitratireducens’ and anammox bacteria, with the former species mediating nitrate-driven oxidation of SCGAs, supplying the latter with nitrite for the oxidation of ammonium. The elimination of nitrite accumulation by the anammox substantially increased SCGA and nitrate consumption rates, whereas suppressing DNRA. Removing ammonium supply led to its eventual production, the accumulation of nitrite, and the upregulation of DNRA gene expression for the abundant ‘Ca. A. nitratireducens’. Increasing the supply of SCGA had a similar effect in promoting DNRA. Our results suggest that ‘Ca. A. nitratireducens’ switches to DNRA to alleviate oxidative stress caused by nitrite accumulation, giving further insight into adaptability and ecology of this microorganism. Our findings also have important implications for the understanding of the fate of nitrogen and SCGAs in anaerobic environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"56 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140603758","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}
Zachary K Garvin, Sebastian R Abades, Nicole Trefault, Fernando D Alfaro, Katie Sipes, Karen G Lloyd, Tullis C Onstott
High-elevation arid regions harbor microbial communities reliant on metabolic niches and flexibility to survive under biologically stressful conditions, including nutrient limitation that necessitates the utilization of atmospheric trace gases as electron donors. Geothermal springs present “oases” of microbial activity, diversity, and abundance by delivering water and substrates, including reduced gases. However, it is unknown whether these springs exhibit a gradient of effects, increasing the spatial reach of their impact on trace gas-oxidizing microbes in the surrounding soils. This study assessed whether proximity to Polloquere, a high-altitude geothermal spring in an Andean salt flat, alters the diversity and metabolic structure of nearby soil bacterial populations compared to the surrounding cold desert. Recovered DNA quantities and metagenomic analyses indicate that the spring represents an oasis for microbes in this challenging environment, supporting greater biomass with more diverse metabolic functions in proximal soils that declines sharply with radial distance from the spring. Despite the sharp decrease in biomass, potential rates of atmospheric hydrogen (H2) and carbon monoxide (CO) uptake increase away from the spring. Kinetic estimates suggest that this activity is due to high-affinity trace gas consumption, likely as a survival strategy for energy and/or carbon acquisition. These results demonstrate that Polloquere regulates a gradient of diverse microbial communities and metabolisms, culminating in increased activity of trace gas-oxidizers as the influence of the spring yields to that of the regional salt flat environment. This suggests that the spring holds local importance within the context of the broader salt flat and potentially represents a model ecosystem for other geothermal systems in high-altitude desert environments.
高海拔干旱地区蕴藏着微生物群落,这些群落依靠新陈代谢龛位和灵活性在生物压力条件下生存,其中包括养分限制,因此必须利用大气中的痕量气体作为电子供体。地热泉通过提供水和基质(包括还原气体),为微生物的活动、多样性和丰富性提供了 "绿洲"。然而,这些泉水是否会产生梯度效应,从而扩大对周围土壤中痕量气体氧化微生物的影响范围,目前尚不得而知。本研究评估了与周围的寒冷沙漠相比,靠近安第斯盐滩的高海拔地热泉 Polloquere 是否会改变附近土壤细菌种群的多样性和代谢结构。回收的 DNA 数量和元基因组分析表明,在这一充满挑战的环境中,泉水是微生物的绿洲,它支持近距离土壤中生物量更大、代谢功能更多样化的细菌群落,而随着与泉水的径向距离的增加,生物量急剧下降。尽管生物量急剧下降,但大气中氢(H2)和一氧化碳(CO)的潜在吸收率却在远离泉眼的地方上升。动力学估计表明,这种活动是由于高亲和性痕量气体的消耗,很可能是一种获取能量和/或碳的生存策略。这些结果表明,Polloquere 调节着各种微生物群落和新陈代谢的梯度,当泉水的影响减弱到区域盐滩环境的影响时,痕量气体氧化剂的活动会增加。这表明,在更广阔的盐滩环境中,该泉水在当地具有重要意义,并有可能成为高海拔沙漠环境中其他地热系统的示范生态系统。
{"title":"Prevalence of trace gas-oxidizing soil bacteria increases with radial distance from Polloquere hot spring within a high-elevation Andean cold desert","authors":"Zachary K Garvin, Sebastian R Abades, Nicole Trefault, Fernando D Alfaro, Katie Sipes, Karen G Lloyd, Tullis C Onstott","doi":"10.1093/ismejo/wrae062","DOIUrl":"https://doi.org/10.1093/ismejo/wrae062","url":null,"abstract":"High-elevation arid regions harbor microbial communities reliant on metabolic niches and flexibility to survive under biologically stressful conditions, including nutrient limitation that necessitates the utilization of atmospheric trace gases as electron donors. Geothermal springs present “oases” of microbial activity, diversity, and abundance by delivering water and substrates, including reduced gases. However, it is unknown whether these springs exhibit a gradient of effects, increasing the spatial reach of their impact on trace gas-oxidizing microbes in the surrounding soils. This study assessed whether proximity to Polloquere, a high-altitude geothermal spring in an Andean salt flat, alters the diversity and metabolic structure of nearby soil bacterial populations compared to the surrounding cold desert. Recovered DNA quantities and metagenomic analyses indicate that the spring represents an oasis for microbes in this challenging environment, supporting greater biomass with more diverse metabolic functions in proximal soils that declines sharply with radial distance from the spring. Despite the sharp decrease in biomass, potential rates of atmospheric hydrogen (H2) and carbon monoxide (CO) uptake increase away from the spring. Kinetic estimates suggest that this activity is due to high-affinity trace gas consumption, likely as a survival strategy for energy and/or carbon acquisition. These results demonstrate that Polloquere regulates a gradient of diverse microbial communities and metabolisms, culminating in increased activity of trace gas-oxidizers as the influence of the spring yields to that of the regional salt flat environment. This suggests that the spring holds local importance within the context of the broader salt flat and potentially represents a model ecosystem for other geothermal systems in high-altitude desert environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"17 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140603756","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}
The gut microbiota of insects has been shown to regulate host detoxification enzymes. However, the potential regulatory mechanisms involved remain unknown. Here, we report that gut bacteria increase insecticide resistance by activating the cap “n” collar isoform-C (CncC) pathway through enzymatically generated reactive oxygen species (ROS) in Bactrocera dorsalis. We demonstrated that Enterococcus casseliflavus and Lactococcus lactis, two lactic acid (LA)-producing bacteria, increase the resistance of B. dorsalis to β-cypermethrin by regulating cytochrome P450 (P450) enzymes and α-glutathione S-transferase (GST) activities. These gut symbionts also induced the expression of CncC and muscle aponeurosis fibromatosis (Maf). BdCncC knockdown led to a decrease in resistance caused by gut bacteria. Ingestion of the ROS scavenger vitamin C (VC) in resistant strain (RS) affected the expression of BdCncC/BdKeap1/BdMafK, resulting in reduced P450 and GST activity. Furthermore, feeding with E. casseliflavus or L. lactis showed that BdNOX5 increased ROS production, and BdNOX5 knockdown affected the expression of the BdCncC/BdMafK pathway and detoxification genes. Moreover, LA feeding activated the ROS-associated regulation of P450 and GST activity. Collectively, our findings indicate that symbiotic gut bacteria modulate intestinal detoxification pathways by affecting physiological biochemistry, thus providing new insights into the involvement of insect gut microbes in the development of insecticide resistance.
{"title":"Lactic acid bacteria modulate the CncC pathway to enhance resistance to β-cypermethrin in the oriental fruit fly","authors":"Tian Zeng, Qianyan Fu, Fangyi Luo, Jian Dai, Rong Fu, Yixiang Qi, Xiaojuan Deng, Yongyue Lu, Yijuan Xu","doi":"10.1093/ismejo/wrae058","DOIUrl":"https://doi.org/10.1093/ismejo/wrae058","url":null,"abstract":"The gut microbiota of insects has been shown to regulate host detoxification enzymes. However, the potential regulatory mechanisms involved remain unknown. Here, we report that gut bacteria increase insecticide resistance by activating the cap “n” collar isoform-C (CncC) pathway through enzymatically generated reactive oxygen species (ROS) in Bactrocera dorsalis. We demonstrated that Enterococcus casseliflavus and Lactococcus lactis, two lactic acid (LA)-producing bacteria, increase the resistance of B. dorsalis to β-cypermethrin by regulating cytochrome P450 (P450) enzymes and α-glutathione S-transferase (GST) activities. These gut symbionts also induced the expression of CncC and muscle aponeurosis fibromatosis (Maf). BdCncC knockdown led to a decrease in resistance caused by gut bacteria. Ingestion of the ROS scavenger vitamin C (VC) in resistant strain (RS) affected the expression of BdCncC/BdKeap1/BdMafK, resulting in reduced P450 and GST activity. Furthermore, feeding with E. casseliflavus or L. lactis showed that BdNOX5 increased ROS production, and BdNOX5 knockdown affected the expression of the BdCncC/BdMafK pathway and detoxification genes. Moreover, LA feeding activated the ROS-associated regulation of P450 and GST activity. Collectively, our findings indicate that symbiotic gut bacteria modulate intestinal detoxification pathways by affecting physiological biochemistry, thus providing new insights into the involvement of insect gut microbes in the development of insecticide resistance.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"248 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-04-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140556515","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}
Lingrui Qu, Chao Wang, Stefano Manzoni, Marina Dacal, Fernando T Maestre, Edith Bai
Ongoing global warming is expected to augment soil respiration by increasing microbial activity, driving self-reinforcing feedback to climate change. However, the compensatory thermal adaptation of soil microorganisms and substrate depletion may weaken the effects of rising temperature on soil respiration. To test this hypothesis, we collected soils along a large-scale forest transect in eastern China spanning a natural temperature gradient, and incubated the soils at different temperatures with or without substrate addition. We combined the exponential thermal response function and a data-driven model to study the interaction effect of thermal adaptation and substrate availability on microbial respiration and compared our results to those from two additional continental and global independent datasets. Modelled results suggested that the effect of thermal adaptation on microbial respiration was greater in areas with higher mean annual temperatures, consistent with the compensatory response to warming. In addition, the effect of thermal adaptation on microbial respiration was greater under substrate addition than under substrate depletion, which was also true for the independent datasets reanalyzed using our approach. Our results indicate that thermal adaptation in warmer regions could exert a more pronounced negative impact on microbial respiration when substrate availability is abundant. These findings improve the body of knowledge on how substrate availability influences soil microbial community-temperature interactions, which could improve estimates of projected soil carbon losses to the atmosphere through respiration.
{"title":"Stronger compensatory thermal adaptation of soil microbial respiration with higher substrate availability","authors":"Lingrui Qu, Chao Wang, Stefano Manzoni, Marina Dacal, Fernando T Maestre, Edith Bai","doi":"10.1093/ismejo/wrae025","DOIUrl":"https://doi.org/10.1093/ismejo/wrae025","url":null,"abstract":"Ongoing global warming is expected to augment soil respiration by increasing microbial activity, driving self-reinforcing feedback to climate change. However, the compensatory thermal adaptation of soil microorganisms and substrate depletion may weaken the effects of rising temperature on soil respiration. To test this hypothesis, we collected soils along a large-scale forest transect in eastern China spanning a natural temperature gradient, and incubated the soils at different temperatures with or without substrate addition. We combined the exponential thermal response function and a data-driven model to study the interaction effect of thermal adaptation and substrate availability on microbial respiration and compared our results to those from two additional continental and global independent datasets. Modelled results suggested that the effect of thermal adaptation on microbial respiration was greater in areas with higher mean annual temperatures, consistent with the compensatory response to warming. In addition, the effect of thermal adaptation on microbial respiration was greater under substrate addition than under substrate depletion, which was also true for the independent datasets reanalyzed using our approach. Our results indicate that thermal adaptation in warmer regions could exert a more pronounced negative impact on microbial respiration when substrate availability is abundant. These findings improve the body of knowledge on how substrate availability influences soil microbial community-temperature interactions, which could improve estimates of projected soil carbon losses to the atmosphere through respiration.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"41 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-02-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139728099","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}
Isabella T Ritchie, Brayan Vilanova-Cuevas, Ashley Altera, Kaileigh Cornfield, Ceri Evans, James S Evans, Maria Hopson-Fernandes, Christina A Kellogg, Elayne Looker, Oliver Taylor, Ian Hewson, Mya Breitbart
Mass mortality of the dominant coral reef herbivore Diadema antillarum in the Caribbean in the early 1980s led to a persistent phase shift from coral- to algal-dominated reefs. In 2022, a scuticociliate most closely related to Philaster apodigitiformis caused further mass mortality of D. antillarum across the Caribbean, leading to >95% mortality at affected sites. Mortality was also reported in the related species Diadema setosum in the Mediterranean in 2022, where urchins experienced gross signs compatible with scuticociliatosis. However, the causative agent of the Mediterranean outbreak has not yet been determined. In April 2023, mass mortality of D. setosum occurred along the Sultanate of Oman’s coastline. Urchins displayed signs compatible with scuticociliatosis including abnormal behavior, drooping and loss of spines, followed by tissue necrosis and death. Here we report the detection of an 18S rRNA gene sequence in abnormal urchins from Muscat, Oman that is identical to the Philaster strain responsible for D. antillarum mass mortality in the Caribbean. We also show that scuticociliatosis signs can be elicited in D. setosum by experimental challenge with the cultivated Philaster strain associated with Caribbean scuticociliatosis. These results demonstrate the Philaster sp. associated with D. antillarum mass mortality has rapidly spread to geographically distant coral reefs, compelling global-scale awareness and monitoring for this devastating condition through field surveys, microscopy, and molecular microbiological approaches, and prompting investigation of long-range transmission mechanisms.
{"title":"Transglobal spread of an ecologically relevant sea urchin parasite","authors":"Isabella T Ritchie, Brayan Vilanova-Cuevas, Ashley Altera, Kaileigh Cornfield, Ceri Evans, James S Evans, Maria Hopson-Fernandes, Christina A Kellogg, Elayne Looker, Oliver Taylor, Ian Hewson, Mya Breitbart","doi":"10.1093/ismejo/wrae024","DOIUrl":"https://doi.org/10.1093/ismejo/wrae024","url":null,"abstract":"Mass mortality of the dominant coral reef herbivore Diadema antillarum in the Caribbean in the early 1980s led to a persistent phase shift from coral- to algal-dominated reefs. In 2022, a scuticociliate most closely related to Philaster apodigitiformis caused further mass mortality of D. antillarum across the Caribbean, leading to >95% mortality at affected sites. Mortality was also reported in the related species Diadema setosum in the Mediterranean in 2022, where urchins experienced gross signs compatible with scuticociliatosis. However, the causative agent of the Mediterranean outbreak has not yet been determined. In April 2023, mass mortality of D. setosum occurred along the Sultanate of Oman’s coastline. Urchins displayed signs compatible with scuticociliatosis including abnormal behavior, drooping and loss of spines, followed by tissue necrosis and death. Here we report the detection of an 18S rRNA gene sequence in abnormal urchins from Muscat, Oman that is identical to the Philaster strain responsible for D. antillarum mass mortality in the Caribbean. We also show that scuticociliatosis signs can be elicited in D. setosum by experimental challenge with the cultivated Philaster strain associated with Caribbean scuticociliatosis. These results demonstrate the Philaster sp. associated with D. antillarum mass mortality has rapidly spread to geographically distant coral reefs, compelling global-scale awareness and monitoring for this devastating condition through field surveys, microscopy, and molecular microbiological approaches, and prompting investigation of long-range transmission mechanisms.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"221 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-02-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139716983","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}
Mira D Liu, Yongle Du, Sara K Koupaei, Nicole R Kim, Monika S Fischer, Wenjun Zhang, Matthew F Traxler
Wildfires affect soils in multiple ways, leading to numerous challenges for colonizing microorganisms. While it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largely unknown. Through bioactivity screening of bacterial isolates from burned soils, we discovered that several Paraburkholderia spp. isolates produced a set of unusual rhamnolipid surfactants with a natural methyl ester modification. These rhamnolipid methyl esters (RLMEs) exhibited enhanced antimicrobial activity against other postfire microbial isolates, including pyrophilous Pyronema fungi and Amycolatopsis bacteria, compared to the typical rhamnolipids made by organisms such as Pseudomonas spp. RLMEs also showed enhanced surfactant properties and facilitated bacterial motility on agar surfaces. In vitro assays further demonstrated that RLMEs improved aqueous solubilization of polycyclic aromatic hydrocarbons, which are potential carbon sources found in char. Identification of the rhamnolipid biosynthesis genes in the postfire isolate, Paraburkholderia kirstenboschensis str. F3, led to the discovery of rhlM, whose gene product is responsible for the unique methylation of rhamnolipid substrates. RhlM is the first characterized bacterial representative of a large class of integral membrane methyltransferases that are widespread in bacteria. These results indicate multiple roles for RLMEs in the postfire lifestyle of Paraburkholderia isolates, including enhanced dispersal, solubilization of potential nutrients, and inhibition of competitors. Our findings shed new light on the chemical adaptations that bacteria employ to navigate, grow, and outcompete other soil community members in postfire environments.
{"title":"Surface-active antibiotic production as a multifunctional adaptation for postfire microorganisms","authors":"Mira D Liu, Yongle Du, Sara K Koupaei, Nicole R Kim, Monika S Fischer, Wenjun Zhang, Matthew F Traxler","doi":"10.1093/ismejo/wrae022","DOIUrl":"https://doi.org/10.1093/ismejo/wrae022","url":null,"abstract":"Wildfires affect soils in multiple ways, leading to numerous challenges for colonizing microorganisms. While it is thought that fire-adapted microorganisms lie at the forefront of postfire ecosystem recovery, the specific strategies that these organisms use to thrive in burned soils remain largely unknown. Through bioactivity screening of bacterial isolates from burned soils, we discovered that several Paraburkholderia spp. isolates produced a set of unusual rhamnolipid surfactants with a natural methyl ester modification. These rhamnolipid methyl esters (RLMEs) exhibited enhanced antimicrobial activity against other postfire microbial isolates, including pyrophilous Pyronema fungi and Amycolatopsis bacteria, compared to the typical rhamnolipids made by organisms such as Pseudomonas spp. RLMEs also showed enhanced surfactant properties and facilitated bacterial motility on agar surfaces. In vitro assays further demonstrated that RLMEs improved aqueous solubilization of polycyclic aromatic hydrocarbons, which are potential carbon sources found in char. Identification of the rhamnolipid biosynthesis genes in the postfire isolate, Paraburkholderia kirstenboschensis str. F3, led to the discovery of rhlM, whose gene product is responsible for the unique methylation of rhamnolipid substrates. RhlM is the first characterized bacterial representative of a large class of integral membrane methyltransferases that are widespread in bacteria. These results indicate multiple roles for RLMEs in the postfire lifestyle of Paraburkholderia isolates, including enhanced dispersal, solubilization of potential nutrients, and inhibition of competitors. Our findings shed new light on the chemical adaptations that bacteria employ to navigate, grow, and outcompete other soil community members in postfire environments.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"10 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-02-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139700852","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}
Ana Popovic, Eric Yixiao Cao, Joanna Han, Nirvana Nursimulu, Eliza V C Alves-Ferreira, Kyle Burrows, Andrea Kennard, Noor Alsmadi, Michael E Grigg, Arthur Mortha, John Parkinson
Commensal protists and gut bacterial communities exhibit complex relationships, mediated at least in part through host immunity. To improve our understanding of this tripartite interplay, we investigated community and functional dynamics between the murine protist Tritrichomonas musculus (Tmu) and intestinal bacteria in healthy and B cell-deficient mice. We identified dramatic, protist-driven remodeling of resident microbiome growth and activities, in parallel with Tmu functional changes, which were accelerated in the absence of B cells. Metatranscriptomic data revealed nutrient-based competition between bacteria and the protist. Single cell transcriptomics identified distinct Tmu life stages, providing new evidence for trichomonad sexual replication and the formation of pseudocysts. Unique cell states were validated in situ through microscopy and flow cytometry. Our results reveal complex microbial dynamics during the establishment of a commensal protist in the gut, and provide valuable datasets to drive future mechanistic studies.
共生原生动物和肠道细菌群落之间的关系很复杂,至少部分是通过宿主免疫力来调节的。为了加深我们对这种三方相互作用的理解,我们研究了健康小鼠和 B 细胞缺陷小鼠体内小鼠原生动物麝香蓟马(Tritrichomonas musculus,Tmu)与肠道细菌之间的群落和功能动态。我们发现了原生动物驱动的常驻微生物群生长和活动的巨大重塑,与此同时,Tmu 的功能也发生了变化,在缺乏 B 细胞的情况下,这种变化会加速。元转录组数据揭示了细菌与原生动物之间基于营养的竞争。单细胞转录组学确定了不同的 Tmu 生命阶段,为滴虫的有性复制和假囊的形成提供了新的证据。通过显微镜和流式细胞术对独特的细胞状态进行了原位验证。我们的研究结果揭示了一种共生原生动物在肠道建立过程中复杂的微生物动态,并为推动未来的机理研究提供了宝贵的数据集。
{"title":"Commensal protist Tritrichomonas musculus exhibits a dynamic life cycle that induces extensive remodeling of the gut microbiota","authors":"Ana Popovic, Eric Yixiao Cao, Joanna Han, Nirvana Nursimulu, Eliza V C Alves-Ferreira, Kyle Burrows, Andrea Kennard, Noor Alsmadi, Michael E Grigg, Arthur Mortha, John Parkinson","doi":"10.1093/ismejo/wrae023","DOIUrl":"https://doi.org/10.1093/ismejo/wrae023","url":null,"abstract":"Commensal protists and gut bacterial communities exhibit complex relationships, mediated at least in part through host immunity. To improve our understanding of this tripartite interplay, we investigated community and functional dynamics between the murine protist Tritrichomonas musculus (Tmu) and intestinal bacteria in healthy and B cell-deficient mice. We identified dramatic, protist-driven remodeling of resident microbiome growth and activities, in parallel with Tmu functional changes, which were accelerated in the absence of B cells. Metatranscriptomic data revealed nutrient-based competition between bacteria and the protist. Single cell transcriptomics identified distinct Tmu life stages, providing new evidence for trichomonad sexual replication and the formation of pseudocysts. Unique cell states were validated in situ through microscopy and flow cytometry. Our results reveal complex microbial dynamics during the establishment of a commensal protist in the gut, and provide valuable datasets to drive future mechanistic studies.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"17 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-02-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139700815","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}
Huaming Wu, Xingqiang Wu, Lorenzo Rovelli, Andreas Lorke
Prediction of the complex cyanobacteria-environment interactions is vital for understanding harmful bloom formation. Most previous studies on these interactions considered specific properties of cyanobacterial cells as representative for the entire population (e.g., growth rate, mortality, and photosynthetic capacity (Pmax)), and assumed that they remained spatiotemporally unchanged. Although, at the population level, the alteration of such traits can be driven by intraspecific competition, little is known about how traits and their plasticity change in response to environmental conditions and affect the bloom formation. Here we test the hypothesis that intraspecific variations in Pmax of cyanobacteria (Microcystis spp.) play an important role in its population dynamics. We coupled a one-dimensional hydrodynamic model with a trait-based phytoplankton model to simulate the effects of physical drivers (turbulence and turbidity) on the Pmax of Microcystis populations for a range of dynamic conditions typical for shallow eutrophic lakes. Our results revealed that turbulence acts as a directional selective driver for changes in Pmax. Depending on the intensity of daily-periodic turbulence, representing wind-driven mixing, a shift in population-averaged phenotypes occurred toward either low Pmax, allowing the population to capture additional light in the upper layers, or high Pmax, enhancing the efficiency of light utilization. Moreover, we observed that a high intraspecific diversity in Pmax accelerated the formation of surface scum by up to more than four times compared to a lower diversity. This study offers insights into mechanisms by which cyanobacteria populations respond to turbulence and underscores the significance of intraspecific variations in cyanobacterial bloom formation. Highlights
{"title":"Selection of photosynthetic traits by turbulent mixing governs formation of cyanobacterial blooms in shallow eutrophic lakes","authors":"Huaming Wu, Xingqiang Wu, Lorenzo Rovelli, Andreas Lorke","doi":"10.1093/ismejo/wrae021","DOIUrl":"https://doi.org/10.1093/ismejo/wrae021","url":null,"abstract":"Prediction of the complex cyanobacteria-environment interactions is vital for understanding harmful bloom formation. Most previous studies on these interactions considered specific properties of cyanobacterial cells as representative for the entire population (e.g., growth rate, mortality, and photosynthetic capacity (Pmax)), and assumed that they remained spatiotemporally unchanged. Although, at the population level, the alteration of such traits can be driven by intraspecific competition, little is known about how traits and their plasticity change in response to environmental conditions and affect the bloom formation. Here we test the hypothesis that intraspecific variations in Pmax of cyanobacteria (Microcystis spp.) play an important role in its population dynamics. We coupled a one-dimensional hydrodynamic model with a trait-based phytoplankton model to simulate the effects of physical drivers (turbulence and turbidity) on the Pmax of Microcystis populations for a range of dynamic conditions typical for shallow eutrophic lakes. Our results revealed that turbulence acts as a directional selective driver for changes in Pmax. Depending on the intensity of daily-periodic turbulence, representing wind-driven mixing, a shift in population-averaged phenotypes occurred toward either low Pmax, allowing the population to capture additional light in the upper layers, or high Pmax, enhancing the efficiency of light utilization. Moreover, we observed that a high intraspecific diversity in Pmax accelerated the formation of surface scum by up to more than four times compared to a lower diversity. This study offers insights into mechanisms by which cyanobacteria populations respond to turbulence and underscores the significance of intraspecific variations in cyanobacterial bloom formation. Highlights","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"51 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-02-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139676879","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}
Elias Broman, Markus Olsson, Adele Maciute, Daniel Donald, Christoph Humborg, Alf Norkko, Tom Jilbert, Stefano Bonaglia, Francisco J A Nascimento
Coastal ecosystems dominate oceanic methane (CH4) emissions. However, there is limited knowledge about how biotic interactions between infauna and aerobic methanotrophs (i.e. CH4 oxidizing bacteria) drive the spatial–temporal dynamics of these emissions. Here, we investigated the role of meio- and macrofauna in mediating CH4 sediment–water fluxes and aerobic methanotrophic activity that can oxidize significant portions of CH4. We show that macrofauna increases CH4 fluxes by enhancing vertical solute transport through bioturbation, but this effect is somewhat offset by high meiofauna abundance. The increase in CH4 flux reduces CH4 pore-water availability, resulting in lower abundance and activity of aerobic methanotrophs, an effect that counterbalances the potential stimulation of these bacteria by higher oxygen flux to the sediment via bioturbation. These findings indicate that a larger than previously thought portion of CH4 emissions from coastal ecosystems is due to faunal activity and multiple complex interactions with methanotrophs.
{"title":"Biotic interactions between benthic infauna and aerobic methanotrophs mediate methane fluxes from coastal sediments","authors":"Elias Broman, Markus Olsson, Adele Maciute, Daniel Donald, Christoph Humborg, Alf Norkko, Tom Jilbert, Stefano Bonaglia, Francisco J A Nascimento","doi":"10.1093/ismejo/wrae013","DOIUrl":"https://doi.org/10.1093/ismejo/wrae013","url":null,"abstract":"Coastal ecosystems dominate oceanic methane (CH4) emissions. However, there is limited knowledge about how biotic interactions between infauna and aerobic methanotrophs (i.e. CH4 oxidizing bacteria) drive the spatial–temporal dynamics of these emissions. Here, we investigated the role of meio- and macrofauna in mediating CH4 sediment–water fluxes and aerobic methanotrophic activity that can oxidize significant portions of CH4. We show that macrofauna increases CH4 fluxes by enhancing vertical solute transport through bioturbation, but this effect is somewhat offset by high meiofauna abundance. The increase in CH4 flux reduces CH4 pore-water availability, resulting in lower abundance and activity of aerobic methanotrophs, an effect that counterbalances the potential stimulation of these bacteria by higher oxygen flux to the sediment via bioturbation. These findings indicate that a larger than previously thought portion of CH4 emissions from coastal ecosystems is due to faunal activity and multiple complex interactions with methanotrophs.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"2 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139660138","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}
Esther Rubio-Portillo, Sophia Robertson, Josefa Antón
The increasing trend in sea surface temperature promotes the spread of Vibrio species, which are known to cause diseases in a wide range of marine organisms. Among these pathogens, Vibrio mediterranei has emerged as a significant threat, leading to bleaching in the coral species Oculina patagonica. Bacteriophages, or phages, are viruses that infect bacteria, thereby regulating microbial communities and playing a crucial role in the coral’s defense against pathogens. However, our understanding of phages that infect V. mediterranei is limited. In this study, we identified two phage species capable of infecting V. mediterranei, utilizing a combination of cultivation and metagenomic approaches. These phages are low-abundance specialists within the coral mucus layer that exhibit rapid proliferation in the presence of their hosts, suggesting a potential role in coral defense. Additionally, one of these phages possesses a conserved domain of a leucine-rich repeat protein, similar to those harbored in the coral genome, that plays a key role in pathogen recognition, hinting at potential coral-phage coevolution. Furthermore, our research suggests that lytic Vibrio infections could trigger prophage induction, which may disseminate genetic elements, including virulence factors, in the coral mucus layer. Overall, our findings underscore the importance of historical coral-phage interactions as a form of coral immunity against invasive Vibrio pathogens.
{"title":"Coral mucus as a reservoir of bacteriophages targeting Vibrio pathogens","authors":"Esther Rubio-Portillo, Sophia Robertson, Josefa Antón","doi":"10.1093/ismejo/wrae017","DOIUrl":"https://doi.org/10.1093/ismejo/wrae017","url":null,"abstract":"The increasing trend in sea surface temperature promotes the spread of Vibrio species, which are known to cause diseases in a wide range of marine organisms. Among these pathogens, Vibrio mediterranei has emerged as a significant threat, leading to bleaching in the coral species Oculina patagonica. Bacteriophages, or phages, are viruses that infect bacteria, thereby regulating microbial communities and playing a crucial role in the coral’s defense against pathogens. However, our understanding of phages that infect V. mediterranei is limited. In this study, we identified two phage species capable of infecting V. mediterranei, utilizing a combination of cultivation and metagenomic approaches. These phages are low-abundance specialists within the coral mucus layer that exhibit rapid proliferation in the presence of their hosts, suggesting a potential role in coral defense. Additionally, one of these phages possesses a conserved domain of a leucine-rich repeat protein, similar to those harbored in the coral genome, that plays a key role in pathogen recognition, hinting at potential coral-phage coevolution. Furthermore, our research suggests that lytic Vibrio infections could trigger prophage induction, which may disseminate genetic elements, including virulence factors, in the coral mucus layer. Overall, our findings underscore the importance of historical coral-phage interactions as a form of coral immunity against invasive Vibrio pathogens.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"19 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139660092","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}