ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wrag082
Qin Han, Guanghui Zhu, Chenxi Li, Mingbo Li, Chenyijun Guo, Junwen Liao, Jiaming Zhang, Yongliang Wang, Hui Wang, Yuxuan Hong, Ming Li, Ye Zhu, Yuming Gong, Hongsheng Song, Chao Su, Peiwu Li, Xia Li
{"title":"Massilia strains facilitate root growth and reshape root microbiota through diverse salicylic acid hydrolysis pathways.","authors":"Qin Han, Guanghui Zhu, Chenxi Li, Mingbo Li, Chenyijun Guo, Junwen Liao, Jiaming Zhang, Yongliang Wang, Hui Wang, Yuxuan Hong, Ming Li, Ye Zhu, Yuming Gong, Hongsheng Song, Chao Su, Peiwu Li, Xia Li","doi":"10.1093/ismejo/wrag082","DOIUrl":"10.1093/ismejo/wrag082","url":null,"abstract":"<p><p>Rhizosphere microbiota play an important role in maintaining plant root growth. However, the physiological and molecular basis of microbial regulation of root traits remains poorly understood. Here, we report that Massilia efficiently colonizes roots and promotes root elongation. In particular, the M117 strain of Massilia significantly inhibits salicylic acid (SA)-related immune signaling, which is required for M117-mediated root elongation. M117 can directly degrade SA, thereby reducing SA levels in the roots. Integrated omics reveal the presence of multiple SA hydrolytic pathways in M117. Among them, the NagGHAaAb pathway is strongly induced by SA. This pathway regulates root growth and is nonrandomly distributed across Massilia species. Finally, we show that M117 colonization enriches specific bacterial taxa within roots. Our findings reveal a specific pathway employed by rhizosphere bacteria to colonize roots and promote their growth and highlight a useful microbial strategy and information for balancing host immunity and growth.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13215587/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"148037248","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wrag198
Dalimil Bujdoš, Jens Walter, Paul W O'Toole
{"title":"Genome-wide association analysis reveals specialization to hosts and niches in multiple species of the Lactobacillaceae.","authors":"Dalimil Bujdoš, Jens Walter, Paul W O'Toole","doi":"10.1093/ismejo/wrag198","DOIUrl":"10.1093/ismejo/wrag198","url":null,"abstract":"<p><p>The Lactobacillaceae inhabit diverse environments, but the extent of their habitat adaptation remains unclear and the colonization factors unknown. First, we applied multiple machine learning models to determine if we can distinguish strains of the same species isolated from two different habitats based on their gene content. Surprisingly, we show that no species is differentially adapted to the oral cavity versus the human gut, or food versus the human gut, while only Lactobacillus crispatus showed specialization to the human urogenital system versus human gut. We then asked which species of Lactobacillaceae are habitat-specialized and how they could be identified. Using multiple lifestyle predictors incorporated in logistic regression models, we found that Limosilactobacillus reuteri, Ligilactobacillus ruminis, L. salivarius, L. crispatus, and L. mucosae displayed the highest degrees of host specialization. Applying our microbial genome-wide association study tool, aurora, to these species identified genes encoding adhesins and bacteriocins as the strongest and most common adaptation factors. This work establishes a generalizable framework for identifying novel species-habitat pairs with strong evidence of specialization and for uncovering the genomic features underlying within-species host and habitat adaptation.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13548328/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"148632533","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wrag042
Lukas V F Novak, Lijing Jiang, Marie Hemon, Marilina Fernandez, Léa Russo, Shasha Wang, Zongze Shao, Violette Da Cunha, Karine Alain
{"title":"Sulfur disproportionation occurs globally across anoxic habitats and has multiple mechanisms of independent evolutionary origin.","authors":"Lukas V F Novak, Lijing Jiang, Marie Hemon, Marilina Fernandez, Léa Russo, Shasha Wang, Zongze Shao, Violette Da Cunha, Karine Alain","doi":"10.1093/ismejo/wrag042","DOIUrl":"10.1093/ismejo/wrag042","url":null,"abstract":"<p><p>Microbial sulfur disproportionation is a unique and enigmatic pathway of energy metabolism in bacteria where a single intermediate sulfur species, e.g. elemental sulfur, is simultaneously oxidized and reduced while generating ATP. We do not have a complete picture of the molecular mechanisms underlying microbial sulfur disproportionation and several pathways are likely involved depending on the taxon. This impairs our ability to investigate the evolutionary history, antiquity, taxonomic distribution, and ecological significance of this metabolism. Here we provide a comprehensive overview of all previously proposed candidate genes, translation of some of which is upregulated under sulfur disproportionation conditions, as well as other sulfur-utilizing dissimilatory metabolic pathways, across the diversity of all genomically characterized sulfur-disproportionating bacteria from a wide range of environments, and phylogenetically reconstruct their evolutionary history. We conclude that the MOLY cluster of likely extracellular molybdopterin oxidoreductases and the YTD cluster of mostly uncharacterized proteins are currently the best candidates for sulfur disproportionation markers in Desulfobacterota and Nitrospirota, and confirm previous observations that other taxa likely use different mechanisms. We also show that sulfur disproportionation pathways utilize enzymes from other processes of sulfur metabolism. The most parsimonious scenario for evolutionary origins of MOLY and YTD clusters is their presence already in the last common ancestor of Desulfobacterota, Nitrospirota, and Acidobacteriota, which lived in the Paleoarchean. Our analyses substantially narrow down the field of viable candidate genes and provide directions for future research.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12998232/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"147328035","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wraf287
Ewa Merz, Riley J Hale, Erik Saberski, Kasia M Kenitz, Melissa L Carter, Jeff S Bowman, Andrew D Barton
{"title":"Temperature alters interactions and keystone taxa in the marine microbiome.","authors":"Ewa Merz, Riley J Hale, Erik Saberski, Kasia M Kenitz, Melissa L Carter, Jeff S Bowman, Andrew D Barton","doi":"10.1093/ismejo/wraf287","DOIUrl":"10.1093/ismejo/wraf287","url":null,"abstract":"<p><p>Marine microbes shape global biogeochemical cycles and marine food webs. Although biotic interactions underpin microbial community dynamics, most interactions between wild marine microbes are unknown. Here, we used empirical dynamic modeling to examine a six-year record of coastal microbial community composition to quantify microbial interactions and their changes through time. We found that, on average, marine microbes interact with 20% of other taxa in the community, most interactions are weak (80%), and that positive interactions are more common than negative interactions. Keystone taxa, defined as having disproportionally strong and frequent interactions, were not generally the most abundant taxa. The strength and sign of interactions, as well as the identity of the keystone taxa, varied through time and with changes in water temperature. An increase of 13°C, the dynamic range in water temperature at this location during the observational period, led to a 33% less interactive microbial community and an 11% shift towards more positive interactions. Only a few of the keystone taxa are the most interactive in the community at all times, and we found a temporal succession of keystone taxa. These results reveal that interactions in the marine microbiome are common, more facilitative than previously thought, and highly variable through time.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12822067/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145858906","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wrag193
Noah S B Houpt, Catherine A Hernandez, Paul E Turner
{"title":"Mutations in filamentous bacteriophages spark eco-evolutionary feedbacks in Pseudomonas aeruginosa.","authors":"Noah S B Houpt, Catherine A Hernandez, Paul E Turner","doi":"10.1093/ismejo/wrag193","DOIUrl":"10.1093/ismejo/wrag193","url":null,"abstract":"<p><p>Microbial populations strongly shape their environment, which can re-route adaptation toward organism-generated fitness optima. However, the conditions that promote these eco-evolutionary feedbacks are unclear. Here, we used experimental evolution to test whether high population density, by strengthening niche construction, drives eco-evolutionary feedbacks in the bacterial pathogen Pseudomonas aeruginosa (Pa) MPAO1. We tested for adaptation to organism-modified environments by measuring the relative performance of ancestral and endpoint populations in filtrate generated by each evolutionary line sampled across generations. Contrary to expectations, we found that endpoint populations had higher performance than the ancestral strain in filtrate across nearly all evolutionary lines regardless of population density. This was caused by the emergence of hyperactive filamentous bacterio(phage) mutants during experimental passaging that inhibited the ancestral strain but not endpoint populations in modified media. Hyperactive phages emerged from one of two avirulent prophages in MPAO1's genome (Pf4 or Pf6). Hyperactive phages drove the evolution of phage resistance in bacterial populations via mutations in the type IV pilus (TIVP), the phage's binding receptor. In a follow-up experiment, we showed that these TIVP mutations pleiotropically reduced motility and conferred resistance to a TIVP-targeting virulent phage, both of which are important traits for Pa infection and treatment. Overall, this work suggests that filamentous phage evolution can drive eco-evolutionary feedbacks in bacterial populations, causing phenotypic and genetic changes that would not be anticipated from adaptation to the extrinsic environment alone.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13502202/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"148671127","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wrag136
Michael L Weltzer, Pravas C Roy, Jack Govaerts, Daniel Wall
{"title":"Aggregative chimeric multicellularity in the absence of lethal kin discrimination.","authors":"Michael L Weltzer, Pravas C Roy, Jack Govaerts, Daniel Wall","doi":"10.1093/ismejo/wrag136","DOIUrl":"10.1093/ismejo/wrag136","url":null,"abstract":"<p><p>Aggregative multicellularity is a cooperative strategy used by some microbes. Unlike plant and animal development, which proceeds through clonal expansion from a single progenitor cell, aggregation is susceptible to genetic conflict and cheating, threatening multicellular stability. Myxococcus xanthus and Dictyostelium spp. are soil-dwelling models that form spore-producing fruiting bodies by aggregation upon starvation. Studies of natural M. xanthus fruiting bodies show that this process is confined to clonemates or close relatives, whereas Dictyostelium spp. can form polyclonal fruiting bodies. Here, we examine kin recognition by co-culturing two distantly related M. xanthus strains under vegetative and starvation conditions. We show that strains segregate and antagonize via their type VI secretion systems (T6SS), yielding monoclonal fruiting bodies. In contrast, mixtures of T6SS mutant strains do not antagonize and form chimeric swarms and fruiting bodies with spores from both strains. Nevertheless, within these T6SS mutant swarms and fruiting bodies, strains segregate, thus revealing that nonlethal kin discrimination mechanisms also exist in this species. These findings further suggest that T6SS are a major mediator of lethal kin discrimination between distantly related strains. Thus, lethal kin discrimination ensures homogeneous populations and monoclonal fruiting body development, whereas nonlethal mechanisms play a more subtle and less discriminatory role similar to Dictyostelium spp.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13310138/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"148220421","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wrag106
Mei Xie, Congjuan Xu, Nan Xiang, Tianhua Liao, Xing Liu, Zhiqi Liu, Xiaoyuan Feng, Qian He, Zizhen Liang, Weiqi Wang, Yifan Dai, Lili Yan, Claudia Pogoreutz, Lena Barra, Shannon Wing Ngor Au, Liwen Jiang, Christian R Voolstra, Haiwei Luo
{"title":"Trait-based signatures associated with persistence and thermal benefit in a genomically decayed coral probiotic.","authors":"Mei Xie, Congjuan Xu, Nan Xiang, Tianhua Liao, Xing Liu, Zhiqi Liu, Xiaoyuan Feng, Qian He, Zizhen Liang, Weiqi Wang, Yifan Dai, Lili Yan, Claudia Pogoreutz, Lena Barra, Shannon Wing Ngor Au, Liwen Jiang, Christian R Voolstra, Haiwei Luo","doi":"10.1093/ismejo/wrag106","DOIUrl":"10.1093/ismejo/wrag106","url":null,"abstract":"<p><p>A key bottleneck in microbiome engineering is ensuring long-term host association of introduced microbes. Selecting probiotic candidates based on evolutionary genomic decay signatures of emerging host dependency offers a potential solution. The Ruegeria strain B4 of population MC10, identified by such signatures, showed persistent coral colonization in a companion study. Whether this persistence translates into measurable host benefit compared to other coral-associated Ruegeria strains, and which mechanisms underlie such benefit, remained unknown. Here we directly compare the probiotic efficacy of MC10-B4 against two sympatric Ruegeria strains isolated from the same coral colony and mucus compartment, controlling for host genotype and microenvironment. MC10-B4 inoculation significantly increased heat stress tolerance in the model cnidarian Aiptasia (Exaiptasia diaphana strain H2), outperforming both controls. To understand the mechanistic basis, we characterized the functional profile of MC10-B4 using integrated multi-omics. The MC10 genome is enriched in host-interaction genes, including siderophore-mediated iron acquisition and exopolysaccharide biosynthesis, confirmed phenotypically by iron scavenging and enhanced biofilm formation. Following exposure to coral tissue extract, MC10-B4 underwent a coordinated \"motile-to-sessile\" proteomic reprogramming, downregulating flagellar motor components while upregulating flagellin and biofilm regulators. This response was distinct from that of sympatric relatives, which instead mounted a broad upregulation of nutrient acquisition systems. MC10-B4's functional profile, particularly its oxidative stress sensitivity, contrasts with traits favored in conventional probiotic screens. Our results provide mechanistic insight into traits associated with long-term host association and thermal benefit, validating an evolution-guided approach that prioritizes innate colonization potential over pre-defined laboratory functionalities for rational probiotic design.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13313319/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"147845372","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wrag055
Magdalena Calusinska, Malte Herold, Dominika Klimek, Marie Bertucci, Sébastien Lemaigre, Sébastien Cambier, Simone Zorzan, Céline Leclercq, Jan Dolfing, Maria Westerholm, Bettina Müller, Leila Nasirzadeh, Anna Schnürer, Paul Wilmes, Philippe Delfosse, Xavier Goux
{"title":"Phylum-wide propionate degradation and its potential connection to poly-gamma-glutamate biosynthesis in Candidatus Cloacimonadota phylum.","authors":"Magdalena Calusinska, Malte Herold, Dominika Klimek, Marie Bertucci, Sébastien Lemaigre, Sébastien Cambier, Simone Zorzan, Céline Leclercq, Jan Dolfing, Maria Westerholm, Bettina Müller, Leila Nasirzadeh, Anna Schnürer, Paul Wilmes, Philippe Delfosse, Xavier Goux","doi":"10.1093/ismejo/wrag055","DOIUrl":"10.1093/ismejo/wrag055","url":null,"abstract":"<p><p>The candidate phylum Cloacimonadota is frequently detected in anoxic environments such as anaerobic digestion (AD) reactors, hydrothermal vents, and deep-sea sediments, yet its metabolism remains poorly understood. Metagenomic evidence suggests capacities for amino acid fermentation, carbohydrate degradation, as well as a potential role in syntrophic propionate oxidation (SPO), a key bottleneck in AD. However, a complete methylmalonyl-CoA (mmc) pathway, central to SPO, has not been previously identified in Cloacimonadota genomes. Here, we report results from an acidified lab-scale anaerobic baffled reactor fed with sugar beet pulp, where an increase in the relative abundance of Cloacimonadota correlated with recovery of methanogenesis, resulting in increased methane content in the produced biogas. Metagenomic and metatranscriptomic analyses enabled metabolic reconstruction of the dominant Cloacimonadota operational taxonomic unit (OTU). Furthermore, using a curated database of 204 genome-resolved Cloacimonadota species, we characterized the phylum-level metabolic potential. Comparative genomics revealed alternative proteins, including 2-oxoglutarate:ferredoxin oxidoreductase and aspartate aminotransferase, likely to substitute for missing enzymes in the classical mmc pathway. These proteins were widely distributed and highly conserved across the analyzed Cloacimonadota genomes, suggesting that this variant of the SPO pathway could represent a phylum-specific trait. Moreover, we hypothesize that these alternative pathway steps may link propionate metabolism to protein degradation and poly-γ-glutamate biosynthesis. Network analysis identified the methanogenic archaeon Methanothrix as a potential syntrophic partner, an interaction further supported by propionate-fed enrichment cultures showing co-occurrence of Cloacimonadota and Methanothrix species. Our study sheds light on the Cloacimonadota metabolism, advancing our understanding of their ecological roles and potential for biotechnological applications.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13082233/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"147476242","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
ISME JournalPub Date : 2026-01-14DOI: 10.1093/ismejo/wrag194
{"title":"Correction to: Phage infection fronts trigger early sporulation and viral entrapment in bacterial populations.","authors":"","doi":"10.1093/ismejo/wrag194","DOIUrl":"10.1093/ismejo/wrag194","url":null,"abstract":"","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":"20 1","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13490944/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"148800948","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Multimodular flavobacterial enzymes specialized in coordinated decomposition of cellulose and alginate in brown algal cell walls.","authors":"Fei Xu, Xiao-Hui Sun, Xiao-Dong Zhang, Xiao-Fei Wang, Yan Wang, Hai-Yan Cao, Peng Wang, Jian-Xun Li, Xi-Ying Zhang, Qi-Long Qin, Xiu-Lan Chen, Yu-Zhong Zhang, Yin Chen, Yu-Qiang Zhang","doi":"10.1093/ismejo/wrag112","DOIUrl":"10.1093/ismejo/wrag112","url":null,"abstract":"<p><p>Brown algal cell walls are complex matrices composed primarily of alginate, cellulose, and fucoidan. Their depolymerization is important in marine carbon cycling. Although numerous algal polysaccharide-degrading enzymes have been characterized, most studies focus on breaking down single, purified polysaccharides, leaving the degradation mechanisms of native cell walls containing mixed polysaccharides poorly understood. Here, we report the integrated modular enzymes involved in brown algal cell wall polysaccharide (BACWP) degradation. Using the marine flavobacterium Aquimarina sp. 2-A2 as a model, we isolated a bifunctional enzyme, CelAly, which integrates a glycoside hydrolase family 5 cellulase domain and a polysaccharide lyase family 31 alginate lyase domain within a single polypeptide, enabling the degradation of cellulose and alginate in brown algal cell walls. In vivo relevance of CelAly was confirmed by upregulation of its gene during growth on algal biomass. CelAly also contains three distinctive substrate-binding modules (B1, B2, UKD) that support its multimodular functionality; among these, UKD is notable for its dual substrate-binding capability. CelAly's modular architecture and interdomain flexibility may facilitate coordinated degradation of BACWPs. Bioinformatic analyses and biochemical validation revealed three additional types of such modular enzymes from marine microbes. CelAly and related modular enzymes are strongly associated with marine environments and exhibit conserved modular strategy for substrate recognition and catabolism. Thus, these enzyme architectures represent a previously unrecognized strategy specialized for BACWP decomposition. This study elucidates the unique structural and functional adaptations of the integrated multimodular enzymes and highlights their ecological prevalence among marine bacteria, providing insights into natural biomass decomposition.</p>","PeriodicalId":50271,"journal":{"name":"ISME Journal","volume":" ","pages":""},"PeriodicalIF":10.2,"publicationDate":"2026-01-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC13235733/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"147857541","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}