The ISME JournalPub Date : 2025-05-27DOI: 10.1093/ismejo/wraf101
Estelle E Clerc, Jeremy E Schreier, Jonasz Słomka, Christa B Smith, He Fu, Justin R Seymour, Jean-Baptiste Raina, Mary Ann Moran, Roman Stocker
{"title":"Chemotaxis, growth, and inter-species interactions shape early bacterial community assembly","authors":"Estelle E Clerc, Jeremy E Schreier, Jonasz Słomka, Christa B Smith, He Fu, Justin R Seymour, Jean-Baptiste Raina, Mary Ann Moran, Roman Stocker","doi":"10.1093/ismejo/wraf101","DOIUrl":"https://doi.org/10.1093/ismejo/wraf101","url":null,"abstract":"From the perspective of a marine copiotrophic bacterium, the surface ocean is a mosaic of exploitable hotspots of organic matter released from living and senescing phytoplankton. Bacterial success in exploiting this patchy microscale environment relies on sensing and swimming towards the hotspots, and upon arrival, growing on available substrates. However, the combined effect of chemotaxis and growth rate on bacterial community assembly has never been quantified. Here, we characterized chemotaxis and growth rate responses of seven representative copiotrophic marine bacteria to phytoplankton exometabolites, both for single species and for pairs of species. We compared these results to prediction of a mathematical null model of hotspot community assembly. Our results revealed that the bacterial strains exhibit diverse responses to phytoplankton metabolites, which can act as either signals, substrates, or both. Interactions between bacterial pairs resulted in chemotactic responses or growth rates different from model predictions in all of the 12 pairs tested (92% differed in chemotaxis, 33% in growth). These community dynamics indicate that inter-species interaction is another factor shaping early colonization of metabolite hotspots, with beneficial, detrimental, and neutral associations observed between bacterial species. Such complex ecological interactions impact chemotactic behaviors and growth rates of marine bacteria on resource hotspots, affecting their community compositions and associated functions relevant to the cycling of key elements including carbon.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"17 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144153306","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 ISME JournalPub Date : 2025-05-26DOI: 10.1093/ismejo/wraf106
Uri Sheyn, Kirsten E Poff, John M Eppley, Andy O Leu, Jessica A Bryant, Fuyan Li, Anna E Romano, Andy Burger, Benedetto Barone, Edward F DeLong
{"title":"Mesoscale eddies shape Prochlorococcuscommunity structure and dynamics in the oligotrophic open ocean","authors":"Uri Sheyn, Kirsten E Poff, John M Eppley, Andy O Leu, Jessica A Bryant, Fuyan Li, Anna E Romano, Andy Burger, Benedetto Barone, Edward F DeLong","doi":"10.1093/ismejo/wraf106","DOIUrl":"https://doi.org/10.1093/ismejo/wraf106","url":null,"abstract":"Mesoscale eddies, horizontally rotating currents sometimes referred to as “ocean weather,” influence open ocean macronutrient distributions, primary production, and microbial community structure. Such eddies impact ecosystems like the North Pacific Subtropical Gyre, where year-round thermal stratification limits the mixing of subsurface macronutrients with surface waters. Populations of the dominant primary producer Prochlorococcusin the North Pacific Subtropical Gyre consist of genetic variants with differential adaptive traits to light intensity, temperature, and macronutrient availability. How Prochlorococcuspopulation variants respond to transient, localized environmental changes, however, remains an open question. Leveraging microbial community phylogenetic, metagenomic, and metatranscriptomic data, we report here a consistent, specific enrichment of Prochlorococcushigh-light I ecotypes around the deep chlorophyll maximum in cyclonic eddies, but not adjacent anticyclonic eddies. The shallower deep chlorophyll maximum depths of cyclones had lower temperatures, higher light intensities, and elevated nutrient concentrations compared to adjacent anticyclones, which favored Prochlorococcushigh-light I ecotype proliferation. Prochlorococcushigh-light I ecotypes in the cyclone deep chlorophyll maximum exhibited unique genetic traits related to nitrogen metabolism and were enriched in gene transcripts associated with energy production, cell replication, and proliferation. Prochlorococcusgene transcripts involved in amino acid transport, metabolism, and biosynthesis were also elevated in the cyclone. These results suggest the potential importance of nitrogen metabolism in Prochlorococcushigh-light I ecotype proliferation in cyclonic eddies. Our findings demonstrate how mesoscale eddies shape microbial community structure in the oligotrophic ocean and how Prochlorococcuscommunities respond to short-term localized environmental variability.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"133 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144136760","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 ISME JournalPub Date : 2025-05-23DOI: 10.1093/ismejo/wraf107
Tiffany N Batarseh,Britt Koskella
{"title":"Distinguishing among evolutionary and ecological processes shaping microbiome dynamics.","authors":"Tiffany N Batarseh,Britt Koskella","doi":"10.1093/ismejo/wraf107","DOIUrl":"https://doi.org/10.1093/ismejo/wraf107","url":null,"abstract":"Evolution is defined as the change in allele frequency over time as a result of either neutral processes, such as genetic drift, or as an adaptive process in response to selection. In contrast, ecological dynamics describe changes in population densities, species distributions, species interactions, and/or relative abundances within communities, all of which can also be the result of either stochastic or deterministic processes. Although the distinction between these patterns has long held for plants and animals, microbial community dynamics can blur the line between ecological and evolutionary processes, especially as they can occur on very similar timescales. Despite the importance of differentiating changes occurring within a population or strain from those occurring among populations, many common methodologies used to study microbiomes are not able to differentiate among them. In this review, we summarize the forces known to generate genetic diversity in bacterial genomes and describe the approaches used to study bacterial evolution from simple to more complex systems. We then explore how current methodologies and conceptual understanding can be applied to both understand and differentiate between the ecological and evolutionary processes in microbial communities. By highlighting lessons from longitudinal microbiome studies and experimental evolution, we explore the unique opportunities afforded by newer sequencing approaches and better sequencing resolution. Throughout, we identify the unique and outstanding challenges in studying these processes in microbiome systems and emphasize the great benefits in doing so to move forward our ability to better predict and manipulate microbiomes.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"18 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144122194","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 ISME JournalPub Date : 2025-05-22DOI: 10.1093/ismejo/wraf103
Blake Dirks, Taylor L Davis, Elvis A Carnero, Karen D Corbin, Steven R Smith, Bruce E Rittmann, Rosa Krajmalnik-Brown
{"title":"Methanogenesis associated with altered microbial production of short-chain fatty acids and human-host metabolizable energy","authors":"Blake Dirks, Taylor L Davis, Elvis A Carnero, Karen D Corbin, Steven R Smith, Bruce E Rittmann, Rosa Krajmalnik-Brown","doi":"10.1093/ismejo/wraf103","DOIUrl":"https://doi.org/10.1093/ismejo/wraf103","url":null,"abstract":"Methanogens are methane-producing, hydrogen-oxidizing (i.e., hydrogenotrophic) archaea. Numerous studies have associated methanogens with obesity, but these results have been inconsistent. One link to metabolism may be methanogens’ hydrogen-oxidizing ability, thus reducing hydrogen partial pressure and thermodynamically enhancing fermentation of sugars to short-chain fatty acids that the host can absorb. Because research linking methanogenesis to human metabolism is limited, our goal with this exploratory analysis was to investigate relationships between methanogens and other hydrogenotrophs, along with the association of methanogens with human metabolizable energy. Using results from a randomized crossover feeding study including a western diet and a high-fiber diet, well-characterized human participants, and continuous methane measurements, we analyzed hydrogenotroph abundance and activity, fecal and serum short-chain fatty acids, and host metabolizable energy between high and low methane producers. We detected methanogens in about one-half of participants. We found no evidence that methanogens’ consumption of hydrogen to produce methane affected other hydrogenotrophs. High methane producers had greater serum propionate and greater gene and transcript abundance of a key enzyme of the hydrogen-consuming, propionate-producing succinate pathway. High methane producers also had greater metabolizable energy than low producers on the high-fiber diet. A network analysis revealed positive relationships between the methane-production rate and bacteria capable of degrading fiber and fermenting fiber-degradation products, thus forming a trophic chain to extract additional energy from undigested substrates. Our results show that methanogenesis in a microbial consortium was linked to host metabolizable energy through enhanced microbial production, and subsequent host absorption, of short-chain fatty acids.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"20 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144122570","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 ISME JournalPub Date : 2025-05-22DOI: 10.1093/ismejo/wraf102
Markus Bittlingmaier,Nathalie Séjalon-Delmas,Kezia Goldmann,David Johnson,Raoul Huys,Grégoire T Freschet
{"title":"Plant and soil biodiversity sustain root mycorrhizal fungal richness under drought stress.","authors":"Markus Bittlingmaier,Nathalie Séjalon-Delmas,Kezia Goldmann,David Johnson,Raoul Huys,Grégoire T Freschet","doi":"10.1093/ismejo/wraf102","DOIUrl":"https://doi.org/10.1093/ismejo/wraf102","url":null,"abstract":"Mycorrhizal phenotypes arise from interactions among plants, soil biota, and environmental factors, but disentangling these drivers remains a key challenge in ecology. Understanding how these interactions shape mycorrhizal community assembly and stability is essential for predicting and managing these relationships in both natural and agricultural ecosystems. Here, we designed a fully factorial experiment examining how plant and soil biodiversity impact arbuscular mycorrhizal fungal communities under drought conditions. We further examined the role of plant ecological strategies in shaping these communities by including 16 herbaceous plant species along a gradient of plant-mycorrhizal reliance. Specifically, we investigated how plant traits and functional groups affected root-associated arbuscular mycorrhizal fungal richness and composition. Although drought decreased arbuscular mycorrhizal fungal phylogenetic species richness in roots, this effect was mitigated by higher soil and plant biodiversity. Plants with traits indicating high mycorrhizal reliance, such as legumes, displayed lower arbuscular mycorrhizal fungal richness but maintained higher constancy over time and across treatments. Overall, our findings indicate that ecosystems with limited plant and soil biodiversity partially lose their ability to support diverse arbuscular mycorrhizal root colonization under drought conditions. If repeated, such a loss could have severe implications for both immediate plant functioning and long-term soil health. The varied responses of arbuscular mycorrhizal fungal communities to drought in plants with differing ecological strategies suggest diverse fitness outcomes for plants and their symbionts, underscoring the need to integrate plant-symbiont dynamics into ecosystem management approaches to address global change.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"155 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144114131","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}
{"title":"Complete xylan utilization pathway and regulation mechanisms involved in marine algae degradation by cosmopolitan marine and human gut microbiota","authors":"Hai-Ning Sun, Xiu-Lan Chen, Yan Wang, Yan-Ping Zhu, Zhao-Jie Teng, Hai-Yan Cao, Ting-Ting Xu, Yin Chen, Yu-Zhong Zhang, Fang Zhao","doi":"10.1093/ismejo/wraf085","DOIUrl":"https://doi.org/10.1093/ismejo/wraf085","url":null,"abstract":"β-1,3-xylan, typically found in marine algae as a major cell wall polysaccharide, represents an overlooked pool of organic carbon in global oceans. Whilst our understanding of microbial catabolism of xylans has improved significantly, particularly from biotransformations of terrestrial plant biomass that are typically composed of β-1,4-xylans, knowledge on how microbes utilize β-1,3-xylan remains limited. Here, we describe the discovery of a complete pathway for β-1,3-xylan catabolism and its regulation in a marine bacterium, Vibriosp. EA2. The pathway starts with the extracellular decomposition of β-1,3-xylan by two β-1,3-xylanases into β-1,3-xylooligomers, which are mainly internalized by an ATP-binding cassette transporter. The substrate binding protein of this transporter has an L-shaped substrate binding pocket to preferentially bind β-1,3-xylooligomers. Subsequently, two intracellular β-1,3-xylosidases degrade β-1,3-xylooligomers into fermentable xylose. The pathway is activated by a unique regulator with xylose being the effector. This β-1,3-xylan catabolic pathway differs from that of β-1,4-xylan catabolism in enzymes, transporters, and regulators. Bioinformatic analysis suggests that the β-1,3-xylan catabolism pathway is not only prevalent in diverse marine bacteria and cosmopolitan human gut microbiota, such as Bacteroides, but also likely transferred horizontally from algae-degrading marine bacteria to the human gut.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"16 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144113822","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 ISME JournalPub Date : 2025-05-22DOI: 10.1093/ismejo/wraf094
Md Moinuddin Sheam, Elaine Luo
{"title":"Vertical transport and spatiotemporal dynamics of giant viruses in the North Pacific Subtropical Gyre","authors":"Md Moinuddin Sheam, Elaine Luo","doi":"10.1093/ismejo/wraf094","DOIUrl":"https://doi.org/10.1093/ismejo/wraf094","url":null,"abstract":"Nucleocytoplasmic large DNA viruses, or “giant viruses,” are prevalent in marine environments, infecting diverse eukaryotic lineages and influencing the marine carbon cycle. Their genomes harbor wide range of auxiliary metabolic genes that influence biogeochemical processes. This study integrates planktonic (5–4000 m) and particle-associated (4000 m) metagenomic samples in the North Pacific Subtropical Gyre, along with particulate export flux data at 4000 m, to investigate the vertical transport of giant viruses and their correlation with carbon export through space and time. By analyzing metagenomic samples over a period of 6 years across 15 depths, we curated a database of 37 giant virus population genomes and 1496 contigs and investigated their spatiotemporal variability and functional capacity in the open ocean. We reported multiple lines of evidence supporting the viral shuttle hypothesis, including the vertical transport of giant viruses from the upper ocean to abyssal depths and their positive correlation with particulate carbon export flux at 4000 m, particularly a giant species closely related to Phaeocystis globosavirus known to infect a bloom-forming alga. We identified giant viruses encoding diverse AMGs, including genes associated with photosynthesis, nutrient transport, and energy metabolism. These auxiliary metabolic genes displayed depth-specific distributions, which we postulate reflect depth-specific adaptations to light-energy and nutrient-limited conditions along the water column. Together, this study provides critical insights into the biogeochemical impacts of giant viruses by identifying key giant viruses that can impact export processes and depth-specific distributions of auxiliary metabolic genes impacting biogeochemical processes along the open ocean water column.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"31 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144113823","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 ISME JournalPub Date : 2025-05-22DOI: 10.1093/ismejo/wraf105
Sasha J Kramer,Erin L Jones,Margaret L Estapa,Nicola L Paul,Tatiana A Rynearson,Alyson E Santoro,Sebastian Sudek,Colleen A Durkin
{"title":"Sinking particles exporting diatoms and hacrobia predict the magnitude of oceanic POC flux.","authors":"Sasha J Kramer,Erin L Jones,Margaret L Estapa,Nicola L Paul,Tatiana A Rynearson,Alyson E Santoro,Sebastian Sudek,Colleen A Durkin","doi":"10.1093/ismejo/wraf105","DOIUrl":"https://doi.org/10.1093/ismejo/wraf105","url":null,"abstract":"Carbon flux to the deep sea can be dictated by surface ocean phytoplankton community composition, but translating surface ocean observations into quantitative predictions of carbon export requires additional consideration of the underlying ecosystem drivers. Here, we used genetic tracers of phytoplankton detected in surface seawater and within sinking particles collected in the mesopelagic ocean to identify mechanistic links between surface communities and carbon export in the North Pacific and North Atlantic Oceans. Phytoplankton 18S rRNA gene sequences were sampled over a one-month period in surface seawater and within bulk-collected and individually isolated sinking particles using mesopelagic sediment traps (100-500 m). Nearly all phytoplankton amplicon sequence variants exported from the surface were packaged in large (>300 μm) particles. Individually, each of these particles contained only a few distinct phytoplankton amplicon sequence variants, but collectively, large particles transported about half of the surface taxonomic diversity into the mesopelagic. The relative sequence abundances of the surface community detected within particles were quantitatively related to measured carbon fluxes: a linear model based on the relative sequence abundance of just two pigment-based phytoplankton taxa, diatoms and photosynthetic Hacrobia, was predictive of carbon flux magnitude. These two taxa were also enriched in the ecologically distinct particle classes that had the greatest influence on carbon export magnitude. As global, hyperspectral ocean color satellites begin to quantify these taxonomic groups in the surface ocean, the relationship of these taxa to carbon fluxes demonstrated here may help in developing more accurate algorithms to estimate global carbon export in the ocean.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"237 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144122170","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 ISME JournalPub Date : 2025-05-21DOI: 10.1093/ismejo/wraf100
Jiadong He,Judith Van Dingenen,Sofie Goormachtig,Maryline Calonne-Salmon,Stéphane Declerck
{"title":"Legume-specific recruitment of rhizobia by hyphae of arbuscular mycorrhizal fungi.","authors":"Jiadong He,Judith Van Dingenen,Sofie Goormachtig,Maryline Calonne-Salmon,Stéphane Declerck","doi":"10.1093/ismejo/wraf100","DOIUrl":"https://doi.org/10.1093/ismejo/wraf100","url":null,"abstract":"The legume-rhizobia symbiosis possesses great potential for sustainable agriculture because of its ability to fix atmospheric nitrogen, reducing crop dependence on nitrogen fertilizers. Rhizobia recognize the host legume through flavonoids released by the roots. These signals are detected by bacteria typically over a few millimeters. Recent research has shown that arbuscular mycorrhizal fungi extend this recognition beyond 15 cm by transporting flavonoids along their hyphae. In soil, common mycorrhizal networks linking plants are formed by arbuscular mycorrhizal fungi. We hypothesized that such networks linking different legumes can transmit host-specific signals, guiding rhizobia to their appropriate hosts. Using in vitro and greenhouse microcosms, we linked Medicago truncatula and Glycine max via a common mycorrhizal network of Rhizophagus irregularis and inoculated GFP-labeled Sinorhizobium meliloti and mCherry-labeled Bradyrhizobium diazoefficiens on the hyphae. S. meliloti preferentially migrated towards M. truncatula, whereas B. diazoefficiens preferentially migrated towards G. max (155 ± 8 and 13 ± 3 nodules, respectively). This was confirmed in the greenhouse with a higher concentration of S. meliloti (2.1-2.5 × 105 CFU·g-1) near M. truncatula and a higher concentration of B. diazoefficiens (1.5-1.6 × 105 CFU·g-1) near G. max (71-82 and 15-18 nodules, respectively). Metabolomics revealed host-specific flavonoids in hyphal exudates: M. truncatula-connected hyphae released DL-liquiritigenin, naringenin, sakuranetin, and 3,7-dimethylquercetin, whereas G. max-connected hyphae released daidzin, 6\"-O-malonyldaidzin, irilone, and erylatissin A. These findings establish that common mycorrhizal networks constitute a \"navigation system\", using chemical signals to orient rhizobia towards their specific hosts, thereby improving nodulation with potential applications in agriculture.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"71 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144103753","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 ISME JournalPub Date : 2025-05-20DOI: 10.1093/ismejo/wraf099
Se Hyeon Jang,YuanYu Lin,Adrian Marchetti
{"title":"Distinct iron acquisition strategies in oceanic and coastal variants of the mixotrophic dinoflagellate Karlodinium.","authors":"Se Hyeon Jang,YuanYu Lin,Adrian Marchetti","doi":"10.1093/ismejo/wraf099","DOIUrl":"https://doi.org/10.1093/ismejo/wraf099","url":null,"abstract":"The availability of the micronutrient iron is important in regulating phytoplankton growth across much of the world's oceans, particularly in the high-nutrient, low-chlorophyll regions. Compared to known mechanisms of iron acquisition and conservation in autotrophic protists (e.g., diatoms), those of dinoflagellates remain unclear, despite their frequent presence in offshore iron-limited waters. Here, we investigate the strategies of an ecologically important mixotrophic dinoflagellate to coping with low iron conditions. Coupled gene expression and physiological responses as a function of iron availability were examined in oceanic and coastal strains of the dinoflagellate Karlodinium. Under iron-replete conditions, grazing was only detected in coastal variants, resulting in faster growth rates compared to when grown autotrophically. Under iron-limited conditions, all isolates exhibited slower growth rates, reduced photosynthetic efficiencies, and lower cellular iron quotas than in iron-replete conditions. However, oceanic isolates exhibited higher relative growth rates compared to coastal isolates under similar low iron concentrations, suggesting they are better adapted to coping under iron limitation. Yet the oceanic isolates did not exhibit the ability to appreciably reduce cell volume or increase iron-use efficiencies compared to the coastal isolates to cope with iron limitation, as often observed in oceanic diatoms. Rather, molecular pathway analysis and corresponding gene expression patterns suggest oceanic Karlodiniumutilizes a high-affinity iron uptake system when iron is low. Our findings reveal cellular mechanisms by which dinoflagellates have adapted to low iron conditions, further shedding light on how they potentially survive in variable iron regions of the world's ocean.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"13 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-05-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144103533","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}