Evolutionary Dynamics Research Articles

Rapid radiation of a plant lineage sheds light on the assembly of dry valley biomes.

Southwest China is characterized by high plateaus, large mountain systems, and deeply incised dry valleys formed by major rivers and their tributaries. Despite the considerable attention given to alpine plant radiations in this region, the timing and mode of diversification of the numerous dry valley plant lineages remain unknown. To address this knowledge gap, we investigated the macroevolution of Isodon (Lamiaceae), a lineage commonly distributed in the dry valleys in southwest China and wetter areas of Asia and Africa. We reconstructed a robust phylogeny encompassing nearly 90% of the approximately 140 extant Isodon species using transcriptome and genome-resequencing data. Our results suggest a rapid radiation of Isodon during the Pliocene that coincided with a habit shift from herbs to shrubs and a habitat shift from humid areas to dry valleys. The shrubby growth form likely acted as a preadaptation allowing for the movement of Isodon species into these dry valleys. Ecological analyses highlight drought-related factors as key drivers influencing the niche preferences of different growth forms and species richness of Isodon. The interplay between topography and the development of the East Asian monsoon since the middle Miocene likely contributed to the formation of the dry valley biome in southwest China. This study enhances our understanding of evolutionary dynamics and ecological drivers shaping the distinctive flora of southwest China and reveals the strategies employed by montane plants in response to climate change and dryland expansion, thus facilitating conservation efforts globally.

Vanadium-Dependent Haloperoxidase Gene Evolution in Brown Algae: Evidence for Horizontal Gene Transfer

Compared with green plants, brown algae are characterized by their ability to accumulate iodine, contributing to their ecological adaptability in high-iodide coastal environments. Vanadium-dependent haloperoxidase (V-HPO) is the key enzyme for iodine synthesis. Despite its significance, the evolutionary origin of V-HPO genes remains underexplored. This study investigates the genomic and evolutionary dynamics of V-HPOs in brown algae, focusing on Laminariales species, particularly Saccharina japonica. Genomic analyses revealed the extensive expansion of the V-HPO gene family in brown algae, with 88 V-HPOs identified in S. japonica, surpassing the number in red algae. Phylogenetic analysis demonstrated distinct evolutionary divergence between brown and red algal V-HPOs, with the brown algal clade closely related to bacterial V-HPOs. These findings suggest horizontal gene transfer (HGT) played a key role in acquiring V-HPO genes, particularly from Acidobacteriota, a bacterial phylum known for genomic plasticity. Additionally, enriched active transposable elements were identified around V-HPO genomic clusters, highlighting their role in tandem gene duplications and rapid HGT processes. Expression profiling further revealed dynamic regulation of V-HPOs in response to environmental conditions. This study provides new insights into how HGT has driven kelp genomic adaptations and enhances understanding of marine ecological success and evolutionary processes.

Persistent, Private and Mobile genes: a model for gene dynamics in evolving pangenomes.

The pangenome of a species is the set of all genes carried by at least one member of the species. In bacteria, pangenomes can be much larger than the set of genes carried by a single organism. Many questions remain unanswered regarding the evolutionary forces shaping the patterns of presence/absence of genes in pangenomes of a given species. We introduce a new model for bacterial pangenome evolution along a species phylogeny that explicitly describes the timing of appearance of each gene in the species and accounts for three generic types of gene evolutionary dynamics: persistent genes that are present in the ancestral genome, private genes that are specific to a given clade, and mobile genes that are imported once into the gene pool and then undergo frequent horizontal gene transfers. We call this model the Persistent-Private-Mobile (PPM) model. We develop an algorithm fitting the PPM model and apply it to a dataset of 902 Salmonella enterica genomes. We show that the best fitting model is able to reproduce the global pattern of some multivariate statistics like the gene frequency spectrum and the parsimony vs. frequency plot. Moreover, the gene classification induced by the PPM model allows us to study the position of accessory genes on the chromosome depending on their category, as well as the gene functions that are most present in each category. This work paves the way for a mechanistic understanding of pangenome evolution, and the PPM model developed here could be used for dynamics-aware gene classification.

RNA Virus Discovery Sheds Light on the Virome of a Major Vineyard Pest, the European Grapevine Moth (Lobesia botrana)

The European grapevine moth (Lobesia botrana) poses a significant threat to vineyards worldwide, causing extensive economic losses. While its ecological interactions and control strategies have been well studied, its associated viral diversity remains unexplored. Here, we employ high-throughput sequencing data mining to comprehensively characterize the L. botrana virome, revealing novel and diverse RNA viruses. We characterized four new viral members belonging to distinct families, with evolutionary cues of cypoviruses (Reoviridae), sobemo-like viruses (Solemoviridae), phasmaviruses (Phasmaviridae), and carmotetraviruses (Carmotetraviridae). Phylogenetic analysis of the cypoviruses places them within the genus in affinity with other moth viruses. The bi-segmented and highly divergent sobemo-like virus showed a distinctive evolutionary trajectory of its encoding proteins at the periphery of recently reported invertebrate Sobelivirales. Notably, the presence of a novel phasmavirus, typically associated with mosquitoes, expands the known host range and diversity of this family to moths. Furthermore, the identification of a carmotetravirus branching in the same cluster as the Providence virus, a lepidopteran virus which replicates in plants, raises questions regarding the biological significance of this moth virus to the grapevine host. We further explored viral sequences in several publicly available transcriptomic datasets of the moth, indicating potential prevalence across distinct conditions. These results underscore the existence of a complex virome within L. botrana and lay the foundation for future studies investigating the ecological roles, evolutionary dynamics, and potential biocontrol applications of these viruses in the L. botrana–vineyard ecosystem.

Pangeneric genome analyses reveal the evolution and diversity of the orchid genus Dendrobium.

Orchids constitute one of the most diverse families of angiosperms, yet their genome evolution and diversity remain unclear. Here we construct and analyse chromosome-scale de novo assembled genomes of 17 representative accessions spanning 12 sections in Dendrobium, one of the largest orchid genera. These accessions represent a broad spectrum of phenotypes, lineages and geographical distributions. We first construct haplotype-resolved genomes for a Dendrobium hybrid and uncover haplotypic variations and allelic imbalance in the heterozygous genome, demonstrating the significance of diverse ancestry. At Dendrobium genus-wide scale, we further elucidate phylogenetic relationships, evolutionary dynamics, entire gene repertoire, and the mechanisms of preserving ancient genetic variants and rapid recent genome evolution for habitat adaption. We also showcase distinctive evolutionary trajectories in MADS-box and PEBP families over 28 Ma. These results considerably contribute to unearthing the mystery of orchid origin, evolution and diversification, laying the foundation for efficient use of genetic diversity in breeding.

Hybridization and Introgression in Black Hakes (Merluccius polli and M. senegalensis): Evolutionary Dynamics and Conservation Implications in the Contact Zone Exploited by Multi-Species Fisheries.

Hybridization is relatively common between closely related species that share part of their distribution. Understanding its dynamics is important both for conservation purposes and to determine its role as an evolutionary mechanism. Here we have studied the case of black hakes (Merluccius polli and Merluccius senegalensis) in its contact zone. The area of study is located in the FAO fishing area 34, in Mauritania and Senegal waters, where both species are exploited jointly in multi-species fisheries involving national and foreign fleets. Using a ddRADSeq approach and based on a set of 5820 SNPs and a total of 240 individuals, we identified one F1 hybrid and several backcrossed individuals among 90 M. polli samples and none in 90 M. senegalensis samples obtained in 2020, suggesting unidirectional introgression towards M. polli. Hybridization signals were not found in any of the 60 historical samples from 2000. Excluding the hybrids and developing two separate sets of SNPs (5093 SNPs for M. polli and 2794 SNPs for M. senegalensis), our results detected two distinct genetic clusters within M. polli that show different genetic diversity estimates, with one of the clusters showing a higher potential vulnerability to exploitation. This pattern was observed in both contemporary and historical samples, and both groups presented subtle depth segregation. Moreover, 109 outlier loci were identified between the two groups, that could be developed into molecular markers to further study differentiation between both clusters and contribute to improved stock assessment and management of these important demersal resources.

In silico characterization of defense system hotspots in Acinetobacter spp.

The bacteria-phage arm race drives the evolution of diverse bacterial defenses. This study identifies and characterizes the defense hotspots in Acinetobacter baumannii using a reference-free approach. Among 4383 high-quality genomes, we found a total of 17,430 phage defense systems and with 54.54% concentrated in 21 hotspots. These hotspots exhibit distinct preferences for different defense systems, and co-occurrence patterns suggest synergistic interactions. Additionally, the mobile genetic elements are abundant around these hotspots, likely facilitating horizontal transfer and evolution of defense systems. The number of hotspots increases in species phylogenetically closer to Acinetobacter baumannii, but the number of defense systems per hotspot varies due to particular selective pressures. These findings provide critical insights into the genetic organization of phage defense systems, contributing to a broader understanding of bacterial immunity and the evolutionary dynamics that shape Acinetobacter genomes. This knowledge lays the foundation for developing targeted interventions to combat antibiotic resistance Acinetobacter baumannii.

Evolutionary dynamics of mitochondrial genomes and intracellular transfers among diploid and allopolyploid cotton species

BackgroundPlant mitochondrial genomes (mitogenomes) exhibit extensive structural variation yet extremely low nucleotide mutation rates, phenomena that remain only partially understood. The genus Gossypium, a globally important source of cotton, offers a wealth of long-read sequencing resources to explore mitogenome and plastome variation and dynamics accompanying the evolutionary divergence of its approximately 50 diploid and allopolyploid species.ResultsHere, we assembled 19 mitogenomes from Gossypium species, representing all genome groups (diploids A through G, K, and the allopolyploids AD) based on a uniformly applied strategy. A graph-based mitogenome assembly method revealed more alternative structural conformations than previously recognized, some of which confirmed the mitogenome structure reported in earlier studies on cotton. Using long-read data, we quantified alternative conformations mediated by recombination events between repeats, and phylogenetically informative structural variants were noted. Nucleotide substitution rate comparisons between coding and non-coding regions revealed low mutation rates across the entire mitogenome. Genome-wide mapping of nuclear organellar DNA transfers (NUOTs) in Gossypium revealed a nonrandom distribution of transfers in the nuclear genome. In cotton, the fate of NUOT events varied, with mitochondrion-to-nucleus transfer (NUMT) predominantly retained as short fragments in the nuclear genome, with more plastid sequences integrated into the nucleus. Phylogenetic relationships inferred using different data sets highlighted distinct evolutionary histories among these cellular compartments, providing ancillary evidence relevant to the evolutionary history of Gossypium.ConclusionsA comprehensive analysis of organellar genome variation demonstrates complex structural variation and low mutation rates across the entire mitogenome and reveals the history of organellar genome transfer among the three genomes throughout the cotton genus. The findings enhance our general understanding of mitogenome evolution, comparative organellar and nuclear evolutionary rates, and the history of inter-compartment genomic integration.

BetaAlign: a deep learning approach for multiple sequence alignment.

Multiple sequence alignments are extensively used in biology, from phylogenetic reconstruction to structure and function prediction. Here, we suggest an out-of-the-box approach for the inference of multiple sequence alignments, which relies on algorithms developed for processing natural languages. We show that our AI-based methodology can be trained to align sequences by processing alignments that are generated via simulations, and thus different aligners can be easily generated for datasets with specific evolutionary dynamics attributes. We expect that natural-language processing solutions will replace or augment classic solutions for computing alignments, and more generally, challenging inference tasks in phylogenomics. The multiple sequence alignment (MSA) problem is a fundamental pillar in bioinformatics, comparative genomics, and phylogenetics. Here we characterize and improve BetaAlign, the first deep learning aligner, which substantially deviates from conventional algorithms of alignment computation. BetaAlign draws on natural language processing (NLP) techniques and trains transformers to map a set of unaligned biological sequences to an MSA. We show that our approach is highly accurate, comparable and sometimes better than state-of-the-art alignment tools. We characterize the performance of BetaAlign and the effect of various aspects on accuracy; for example, the size of the training data, the effect of different transformer architectures, and the effect of learning on a subspace of indel-model parameters (subspace learning). We also introduce a new technique that leads to improved performance compared to our previous approach. Our findings further uncover the potential of NLP-based methods for sequence alignment, highlighting that AI-based algorithms can substantially challenge classic approaches in phylogenomics and bioinformatics. Datasets used in this work are available on HuggingFace (Wolf et al., 2020) at: https://huggingface.co/dotan1111. Source code is available at: https://github.com/idotan286/SimulateAlignments. Supplementary data are available at Bioinformatics online.

Unveiling an ancient whole-genome duplication event in Stentor, the model unicellular eukaryotes.

Whole-genome duplication (WGD) events are widespread across eukaryotes and have played a significant role in moulding the genetic architectures of diverse organisms. In the present study, the newly sequenced genome of a giant ciliated protist, Stentor roeselii, provides an opportunity for the analysis of the collinearity and retention of reciprocal best-hit genes between two Stentor species. As a main result, we have unveiled a previously undetected ancient WGD event shaping the genome of its congener, Stentor coeruleus, a model protist used in cytological and evolutionary studies. Genomes of two congeners, S. coeruleus and S. roeselii, are compared and analyzed, revealing that: (i) the former exhibits a much higher retention rate of colinear-gene pairs (28%) than does S. roeselii, and in S. coeruleus, 75% of genes that have a RBH hit in S. roeselii, have paralogs with high amino-acid identity, consistent with a WGD event in the lineage leading to S. coeruleus; (ii) the S. roeselii genome possesses extremely short intergenic regions, implying that the lengths of intergenic regions are under strong selection; (iii) the unique characteristics of introns may have been shaped in the common ancestor of heterotrichs; (iv) gene families that play a role in activities of multiple protein kinases and voltage-gated ion channels expanded rapidly in the ancestor of both taxa, possibly relating to the remarkable regenerative ability in Stentor. This study offers new insights into the evolutionary dynamics of ciliate genomes, with implications for understanding of the processes underlying the evolution of genomic complexity.

Quantifying the Evolutionary Dynamics of Structure and Content in Closely Related E. coli Genomes.

Bacterial genomes primarily diversify via gain, loss, and rearrangement of genetic material in their flexible accessory genome. Yet the dynamics of accessory genome evolution are very poorly understood, in contrast to the core genome where diversification is readily described by mutations and homologous recombination. Here, we tackle this problem for the case of very closely related genomes. We comprehensively describe genome evolution within n=222 genomes of Escherichia coli ST131, which likely shared a common ancestor around 100 years ago. After removing putative recombinant diversity, the total length of the phylogeny is 6,000 core genome substitutions. Within this diversity, we find 22 modifications to core genome synteny and estimate around 2,000 structural changes within the accessory genome, i.e. one structural change for every three core genome substitutions. Sixty-three percent of loci with structural diversity could be resolved into individual gain and loss events with 10-fold more gains than losses, demonstrating a dominance of gains due to insertion sequences and prophage integration. Our results suggest the majority of synteny changes and insertions in our dataset are likely deleterious and only persist for a short time before being removed by purifying selection.

Strain phylogroup and environmental constraints shape Escherichia coli dynamics and diversity over a 20-year human gut time series.

Escherichia coli is an increasingly antibiotic-resistant opportunistic pathogen. Few data are available on its ecological and evolutionary dynamics in its primary commensal niche, the vertebrate gut. Using Illumina and/or Nanopore technologies, we sequenced whole genomes of 210 E. coli isolates from 22 stools sampled during a 20-year period from a healthy man (ED) living in Paris, France. All phylogroups, except C, were represented, with a predominance of B2 (34.3%), followed by A and F (19% each) phylogroups. Thirty-five clones were identified based on their haplogroup and pairwise genomic single nucleotide polymorphism distance and classified in three phenotypes according to their abundance and residence time: 25 sub-dominant/transient (52 isolates), five dominant/transient (48 isolates) and five dominant/resident (110 isolates). Four over five dominant/resident clones belonged to B2 and closely related F phylogroups, whereas sub-dominant/transient clones belonged mainly to B1, A and D phylogroups. The long residence times of B2 clones seemed to be counterbalanced by lower colonization abilities. Clones with larger within-host frequency persisted for longer. By comparing ED strain genomes to a collection of commensal E. coli genomes from 359 French individuals, we identified ED-specific genomic properties including an enrichment in genes involved in a metabolic pathway (mhp cluster) and the presence of a very rare antiviral defense island. The E. coli colonization within the gut microbiota was shaped by both the intrinsic properties of the strain lineages, in particular longer residence of phylogroup B2, and the environmental constraints such as diet or phages.

A pan-genome perspective on the evolutionary dynamics of polyphyly, virulence, and antibiotic resistance in Salmonella enterica serovar Mbandaka highlights emerging threats to public health and food safety posed by cloud gene families.

Salmonella enterica serovar Mbandaka, a prevalent foodborne pathogen, poses a threat to public health but remains poorly understood. We have determined the phylogenomic tree, genetic diversity, virulence, and antimicrobial resistance (AMR) profiles on a large genomic scale to elucidate the evolutionary dynamics within the Mbandaka pan-genome. The polyphyletic nature of this serovar is characterized by two distinct phylogenetic groups and inter-serovar recombination boundaries, that potentially arising from recombination events at the H2-antigen loci. The open pan-genome exhibited a flexible gene repertoire, with numerous cloud gene families involved in virulence and AMR. Extensive gene gain and loss observed at the terminal nodes of the phylogenetic tree indicate that Mbandaka individuals have undergone frequent gene turnover. The resulting changes in virulence and AMR genes potentially pose emerging threats to public health. We explored serovar conversion due to recombination of H-antigen loci, inter-serovar divergences in gene gain and loss, prophage-mediated acquisition of virulence factors, and the role of incompatibility group plasmids in acquiring resistance determinants as key molecular mechanisms driving the pathogenicity and antibiotic resistance of Mbandaka. Our work contributes to a comprehensive understanding of the complex mechanisms of pathogenesis and the ongoing evolutionary arms race with current therapeutic approaches in serovar Mbandaka.

ParetoTracker: Understanding Population Dynamics in Multi-objective Evolutionary Algorithms through Visual Analytics.

Multi-objective evolutionary algorithms (MOEAs) have emerged as powerful tools for solving complex optimization problems characterized by multiple, often conflicting, objectives. While advancements have been made in computational efficiency as well as diversity and convergence of solutions, a critical challenge persists: the internal evolutionary mechanisms are opaque to human users. Drawing upon the successes of explainable AI in explaining complex algorithms and models, we argue that the need to understand the underlying evolutionary operators and population dynamics within MOEAs aligns well with a visual analytics paradigm. This paper introduces ParetoTracker, a visual analytics framework designed to support the comprehension and inspection of population dynamics in the evolutionary processes of MOEAs. Informed by preliminary literature review and expert interviews, the framework establishes a multi-level analysis scheme, which caters to user engagement and exploration ranging from examining overall trends in performance metrics to conducting fine-grained inspections of evolutionary operations. In contrast to conventional practices that require manual plotting of solutions for each generation, ParetoTracker facilitates the examination of temporal trends and dynamics across consecutive generations in an integrated visual interface. The effectiveness of the framework is demonstrated through case studies and expert interviews focused on widely adopted benchmark optimization problems.

An evolutionary dynamics analysis of the plant DEK gene family reveals the role of BnaA02g08940D in drought tolerance

An evolutionary dynamics analysis of the plant DEK gene family reveals the role of BnaA02g08940D in drought tolerance

Evolutionary dynamics of repetitive elements and their relationship with genome size in Acrididae

It is widely accepted that repetitive elements (REs) represent the primary mechanism driving genome size variation across eukaryotes. The observed genome sizes and REs of 59 species within the Acrididae were obtained and characterized. The genome sizes observed ranged from 6.60 pg to 19.35 pg, while the proportion of REs varied from 57.92 % to 83.58 %. The primary contributors were identified as LTR (2.34 % ~ 20.98 %) and LINEs (6.70 % ~ 16.33 %). The results of ancestral reconstruction indicated that the proportion of REs in ancestral nodes was 69.53 %, which suggests that they have undergone extensive genome expansion or contraction. A significant positive correlation was identified between the proportion of REs and genome size. Transposable elements were found to account for approximately 41 % of the observed variation in genome size. Moreover, the LTR was identified as the most significant RE type in relation to genome size expansion within the Acrididae.

A review of the empirical evidence for costs of plasticity in ectothermic animals.

Phenotypic plasticity can represent a vital adaptive response to environmental stressors, including those associated with climate change. Despite its evolutionary advantages, the expression of plasticity varies significantly within and among species, and is likely to be influenced by local environmental conditions. This variability in plasticity has important implications for evolutionary biology and conservation physiology. Theoretical models suggest that plasticity might incur intrinsic fitness costs, although the empirical evidence is inconsistent and there is ambiguity in the term 'cost of plasticity'. Here, we systematically review the literature to investigate the prevalence of costs associated with phenotypic plasticity in ectothermic animals. We categorized studies into those assessing 'costs of phenotype' (trade-offs between different plastic trait values) and 'costs of plasticity' (intrinsic costs of the capacity for plasticity). Importantly, the experimental designs required to detect costs of plasticity are inherently more complex and onerous than those required to detect costs of phenotype. Accordingly, our findings reveal a significant focus on costs of phenotype over costs of plasticity, with the former more frequently detecting costs. Contrary to theoretical expectations, our analysis suggests that costs of plasticity are neither universal nor widespread. This raises questions about the evolutionary dynamics of plasticity, particularly in stable environments. Our analysis underscores the need for precise terminology and methodology in researching costs of plasticity, to avoid conflating costs associated with plastic traits with costs more intrinsic to plasticity. Understanding these nuances is crucial for predicting how species might adapt to rapidly changing environments.

Global phylogeography and antibiotic resistance characteristics of Morganella: An epidemiological, spatial, comparative genomic study.

Morganella morganii has been recognized as an important opportunistic pathogen that is becoming increasingly prevalent worldwide. However, the current global evolutionary dynamics and emergence of ARGs remain obscure. The present study determined the global distribution, genomic classification, phylogeny, and monitor longitudinal resistome changes. During 1900-2024, a total of 1027 non-duplicate Morganella genomes have been reported from 49 countries. The countries with the highest number were China (433), the USA (143), and France (74). Through ANI distance analysis and core genome phylogeny, Morganella was reclassified into six species: M. morganii, M. sibonii, M. chanii, M. laugraudii, M. kristinii, M. psychrotolerans. Further analysis using cgMLST identified 87 distinct genetic clusters and 737 singleton strains, indicating a high level of multi-locus sequence type diversity and local clonal outbreaks. Bayesian evolutionary analysis revealed the most recent common ancestor year and potential global transmission routes. A total of 195 ARGs were carried by Morganella isolates, with each genome containing between 2 and 544 ARGs. The most common ARGs were associated with resistance to the following drug-classes: aminoglycosides, beta-lactam, chloramphenicol, sulfamides, and tetracycline. Twenty-one carbapenemase-encoding genes were identified in 22 countries, with blaNDM-1, blaKPC-2, blaIMP-27, blaOXA-48, blaNDM-5, blaNDM-7, and blaVIM-1 being the most prevalent. Positive correlations were observed between ARGs and mobile genetic elements, like plasmids, ISs, and Tns, indicating frequent mobilization of certain ARGs by different mobile genetic elements (p < 0.05). In conclusion, Morganella isolates that are showing an upward trend in resistance and infection rates warrant a reclassification of their taxonomy and continuous monitoring for resistance.

Effects of punishment driven by inequity aversion on promoting cooperation in public goods games

Unlike traditional punishment mechanisms, which target individuals adopting specific strategies, punishers driven by inequity aversion focus on individuals with higher payoffs. The intensity of punishment varies based on the difference in payoffs. This paper examines the cooperation-promoting effect of this unique punishment mechanism within a structured population. Specifically, we study the evolutionary dynamics of two three-strategy systems in public goods games (PGGs), comprising cooperators, inequity-averse individuals, and defectors. Furthermore, we analyze the spatial dynamics and the evolution of characteristic spatial distributions of strategies to uncover the mechanisms underlying various phases and phase transitions. Our findings indicate that cooperation is enhanced regardless of whether the punishment is enforced by cooperators or defectors. When inequity-averse individuals cooperate in PGGs, punishing defectors at the cluster boundary fosters cooperation. However, mutual punishment among inequity-averse individuals diminishes the efficiency of cooperation promotion. For inequity-averse defectors, low punishment intensity safeguards cooperators from defector invasion, while high punishment intensity against defectors facilitates the spread of cooperation among them.

Distinct response of nitrogen metabolism to exogenous cadmium (Cd) in river sediments with and without Cd contamination history.

The role of metal resistance on nitrogen metabolism function and community resilience against Cd is important for elucidating the evolutionary dynamics of key ecological functions in river ecosystems. In this study, the response of nitrogen transforming function to Cd exposure in river sediments from the Yangtze River Basin with varying levels of heavy metal contamination history (Cd-contaminated and Cd-free sediments) was compared to understand how Cd influenced nitrogen metabolism under varying metal resistance conditions. The results showed that chronic and persistent Cd pollution of sediments caused an elevation of transport efflux metal resistance genes (MRGs) and a reduction in the uptake MRGs, leading to a stronger tolerance to Cd for Cd-contaminated sediment than Cd-free ones. Specifically, denitrification, anaerobic ammonium oxidation (anammox) and dissimilatory nitrate reduction to ammonium (DNRA) respectively responded to Cd through different mechanisms. Exogenous Cd (5-100 mg kg-1) influenced denitrification rates (-70 %-100 % deviation to control group) by regulating key genera (Thiobacillus, Magnetospirillum, Sideroxydans etc.) and gene clusters for denitrification. Both adaptive nature of anammox bacteria and co-regulation of key genera (Candidatus_Scalindua, Candidatus_Jettenia, Planctomyces etc.) and gene hzsA were drivers of differential responses in sediments from various contamination history. Environmental factors rather than contamination history, key genera or genes were probably critical ones determining Cd-resistance in DNRA, being more tolerant to Cd in sediments with higher TOC and NH4+. Stimulation of N2O reduction process (genera Gemmatimonas and Gemmatirosa and genes nosZ) in Cd-contaminated sediments by exogenous Cd lowered N2O emission risk, whereas the reverse was true for Cd-free sediments. These results enrich our understanding about the linkages among MRGs and nitrogen reduction functions in river.