Oceanographic connectivity explains the intra-specific diversity of mangrove forests at global scales.

The distribution of mangrove intra-specific biodiversity can be structured by historical demographic processes that enhance or limit effective population sizes. Oceanographic connectivity (OC) may further structure intra-specific biodiversity by preserving or diluting the genetic signatures of historical changes. Despite its relevance for biogeography and evolution, the role of oceanographic connectivity in structuring the distribution of mangrove's genetic diversity has not been addressed at global scale. Here we ask whether connectivity mediated by ocean currents explains the intra-specific diversity of mangroves. A comprehensive dataset of population genetic differentiation was compiled from the literature. Multigenerational connectivity and population centrality indices were estimated with biophysical modeling coupled with network analyses. The variability explained in genetic differentiation was tested with competitive regression models built upon classical isolation-by-distance (IBD) models considering geographic distance. We show that oceanographic connectivity can explain the genetic differentiation of mangrove populations regardless of the species, region, and genetic marker (significant regression models in 95% of cases, with an average R-square of 0.44 ± 0.23 and Person's correlation of 0.65 ± 0.17), systematically improving IBD models. Centrality indices, providing information on important stepping-stone sites between biogeographic regions, were also important in explaining differentiation (R-square improvement of 0.06 ± 0.07, up to 0.42). We further show that ocean currents produce skewed dispersal kernels for mangroves, highlighting the role of rare long-distance dispersal events responsible for historical settlements. Overall, we demonstrate the role of oceanographic connectivity in structuring mangrove intra-specific diversity. Our findings are critical for mangroves' biogeography and evolution, but also for management strategies considering climate change and genetic biodiversity conservation.

Trehalose along with ABA promotes the salt tolerance of Avicennia marina by regulating Na+ transport.

Mangroves grow in tropical/subtropical intertidal habitats with extremely high salt tolerance. Trehalose and trehalose-6-phosphate (T6P) have an alleviating function against abiotic stress. However, the roles of trehalose in the salt tolerance of salt-secreting mangrove Avicennia marina is not documented. Here, we found that trehalose was significantly accumulated in A. marina under salt treatment. Furthermore, exogenous trehalose can enhance salt tolerance by promoting the Na+ efflux from leaf salt gland and root to reduce the Na+ content in root and leaf. Subsequently, eighteen trehalose-6-phosphate synthase (AmTPS) and 11 trehalose-6-phosphate phosphatase (AmTPP) genes were identified from A. marina genome. Abscisic acid (ABA) responsive elements were predicted in AmTPS and AmTPP promoters by cis-acting elements analysis. We further identified AmTPS9A, as an important positive regulator, that increased the salt tolerance of AmTPS9A-overexpressing Arabidopsis thaliana by altering the expressions of ion transport genes and mediating Na+ efflux from the roots of transgenic A. thaliana under NaCl treatments. In addition, we also found that ABA could promote the accumulation of trehalose, and the application of exogenous trehalose significantly promoted the biosynthesis of ABA in both roots and leaves of A. marina. Ultimately, we confirmed that AmABF2 directly binds to the AmTPS9A promoter in vitro and in vivo. Taken together, we speculated that there was a positive feedback loop between trehalose and ABA in regulating the salt tolerance of A. marina. These findings provide new understanding to the salt tolerance of A. marina in adapting to high saline environment at trehalose and ABA aspects.

NADPH oxidase-dependent H2O2 production mediates salicylic acid-induced salt tolerance in mangrove plant Kandelia obovata by regulating Na+/K+ and redox homeostasis.

Salicylic acid (SA) is known to enhance salt tolerance in plants. However, the mechanism of SA-mediated response to high salinity in halophyte remains unclear. Using electrophysiological and molecular biological methods, we investigated the role of SA in response to high salinity in mangrove species, Kandelia obovata, a typical halophyte. Exposure of K. obovata roots to high salinity resulted in a rapid increase in endogenous SA produced by phenylalanine ammonia lyase pathway. The application of exogenous SA improved the salt tolerance of K. obovata, which depended on the NADPH oxidase-mediated H2O2. Exogenous SA and H2O2 increased Na+ efflux and reduced K+ loss by regulating the transcription levels of Na+ and K+ transport-related genes, thus reducing the Na+/K+ ratio in the salt-treated K. obovata roots. In addition, exogenous SA-enhanced antioxidant enzyme activity and its transcripts, and the expressions of four genes related to AsA-GSH cycle as well, then alleviated oxidative damages in the salt-treated K. obovata roots. However, the above effects of SA could be reversed by diphenyleneiodonium chloride (the NADPH oxidase inhibitor) and paclobutrazol (a SA biosynthesis inhibitor). Collectively, our results demonstrated that SA-induced salt tolerance of K. obovata depends on NADPH oxidase-generated H2O2 that affects Na+/K+ and redox homeostasis in response to high salinity.

Adaptation in Unstable Environments and Global Gene Losses: Small but Stable Gene Networks by the May-Wigner Theory.

Although gene loss is common in evolution, it remains unclear whether it is an adaptive process. In a survey of seven major mangrove clades that are woody plants in the intertidal zones of daily environmental perturbations, we noticed that they generally evolved reduced gene numbers. We then focused on the largest clade of Rhizophoreae and observed the continual gene set reduction in each of the eight species. A great majority of gene losses are concentrated on environmental interaction processes, presumably to cope with the constant fluctuations in the tidal environments. Genes of the general processes for woody plants are largely retained. In particular, fewer gene losses are found in physiological traits such as viviparous seeds, high salinity, and high tannin content. Given the broad and continual genome reductions, we propose the May-Wigner theory (MWT) of system stability as a possible mechanism. In MWT, the most effective solution for buffering continual perturbations is to reduce the size of the system (or to weaken the total genic interactions). Mangroves are unique as immovable inhabitants of the compound environments in the land-sea interface, where environmental gradients (such as salinity) fluctuate constantly, often drastically. Extending MWT to gene regulatory network (GRN), computer simulations and transcriptome analyses support the stabilizing effects of smaller gene sets in mangroves vis-à-vis inland plants. In summary, we show the adaptive significance of gene losses in mangrove plants, including the specific role of promoting phenotype innovation and a general role in stabilizing GRN in unstable environments as predicted by MWT.

Implications of anomalous relative sea-level rise for the peopling of Remote Oceania.

Beginning ~3,500 to 3,300 y B.P., humans voyaged into Remote Oceania. Radiocarbon-dated archaeological evidence coupled with cultural, linguistic, and genetic traits indicates two primary migration routes: a Southern Hemisphere and a Northern Hemisphere route. These routes are separated by low-lying, equatorial atolls that were settled during secondary migrations ~1,000 y later after their exposure by relative sea-level fall from a mid-Holocene highstand. High volcanic islands in the Federated States of Micronesia (Pohnpei and Kosrae) also lie between the migration routes and settlement is thought to have occurred during the secondary migrations despite having been above sea level during the initial settlement of Remote Oceania. We reconstruct relative sea level on Pohnpei and Kosrae using radiocarbon-dated mangrove sediment and show that, rather than falling, there was a ~4.3-m rise over the past ~5,700 y. This rise, likely driven by subsidence, implies that evidence for early settlement could lie undiscovered below present sea level. The potential for earlier settlement invites reinterpretation of migration pathways into Remote Oceania and monument building. The UNESCO World Heritage sites of Nan Madol (Pohnpei) and Leluh (Kosrae) were constructed when relative sea level was ~0.94 m (~770 to 750 y B.P.) and ~0.77 m (~640 to 560 y B.P.) lower than present, respectively. Therefore, it is unlikely that they were originally constructed as islets separated by canals filled with ocean water, which is their prevailing interpretation. Due to subsidence, we propose that these islands and monuments are more vulnerable to future relative sea-level rise than previously identified.

Climate drives coupled regime shifts across subtropical estuarine ecosystems.

Ecological regime shifts are expected to increase this century as climate change propagates cascading effects across ecosystems with coupled elements. Here, we demonstrate that the climate-driven salt marsh-to-mangrove transition does not occur in isolation but is linked to lesser-known oyster reef-to-mangrove regime shifts through the provision of mangrove propagules. Using aerial imagery spanning 82 y, we found that 83% of oyster reefs without any initial mangrove cover fully converted to mangrove islands and that mean (± SD) time to conversion was 29.1 ± 9.6 y. In situ assessments of mangrove islands suggest substantial changes in ecosystem structure during conversion, while radiocarbon dates of underlying reef formation indicate that such transitions are abrupt relative to centuries-old reefs. Rapid transition occurred following release from freezes below the red mangrove (Rhizophora mangle) physiological tolerance limit (-7.3 °C) and after adjacent marsh-to-mangrove conversion. Additional nonclimate-mediated drivers of ecosystem change were also identified, including oyster reef exposure to wind-driven waves. Coupling of regime shifts arises from the growing supply of mangrove propagules from preceding and adjacent marsh-to-mangrove conversion. Climate projections near the mangrove range limit on the Gulf coast of Florida suggest that regime shifts will begin to transform subtropical estuaries by 2070 if propagule supply keeps pace with predicted warming. Although it will become increasingly difficult to maintain extant oyster habitat with tropicalization, restoring oyster reefs in high-exposure settings or active removal of mangrove seedlings could slow the coupled impacts of climate change shown here.

De novo assembly and analysis of Sonneratia ovata genome and population analysis.

Mangroves are an important part of coastal and estuarine ecosystems where they serve as nurseries for marine species and prevent coastal erosion. Here we report the genome of Sonneratia ovata, which is a true mangrove that grows in estuarine environments and can tolerate moderate salt exposure. We sequenced the S. ovata genome and assembled it into chromosome-level scaffolds through the use of Hi-C. The genome is 212.3 Mb and contains 12 chromosomes that range in size from 12.2 to 23.2 Mb. Annotation identified 29,829 genes with a BUSCO completeness of 95.9%. We identified salt genes and found copy number expansion of salt genes such as ADP-ribosylation factor 1, and elongation factor 1-alpha. Population analysis identified a low level of genetic variation and a lack of population structure within S. ovata.

Unraveling the genomic secrets of Tritonibacter mobilis AK171: a plant growth-promoting bacterium isolated from Avicennia marina.

The scarcity of freshwater resources resulting in a significant yield loss presents a pressing challenge in agriculture. To address this issue, utilizing abundantly available saline water could offer a smart solution. In this study, we demonstrate that the genome sequence rhizosphere bacterium Tritonibacter mobilis AK171, a halophilic marine bacterium recognized for its ability to thrive in saline and waterlogged environments, isolated from mangroves, has the remarkable ability to enable plant growth using saline irrigation. AK171 is characterized as rod-shaped cells, displays agile movement in free-living conditions, and adopts a rosette arrangement in static media. Moreover, The qualitative evaluation of PGP traits showed that AK171 could produce siderophores and IAA but could not solubilize phosphate nor produce hydrolytic enzymes it exhibits a remarkable tolerance to high temperatures and salinity. In this study, we conducted a comprehensive genome sequence analysis of T. mobilis AK171 to unravel the genetic mechanisms underlying its plant growth-promoting abilities in such challenging conditions. Our analysis revealed diverse genes and pathways involved in the bacterium's adaptation to salinity and waterlogging stress. Notably, T. mobilis AK171 exhibited a high level of tolerance to salinity and waterlogging through the activation of stress-responsive genes and the production of specific enzymes and metabolites. Additionally, we identified genes associated with biofilm formation, indicating its potential role in establishing symbiotic relationships with host plants. Furthermore, our analysis unveiled the presence of genes responsible for synthesizing antimicrobial compounds, including tropodithietic acid (TDA), which can effectively control phytopathogens. This genomic insight into T. mobilis AK171 provides valuable information for understanding the molecular basis of plant-microbial interactions in saline and waterlogged environments. It offers potential applications for sustainable agriculture in challenging conditions.

Identification and analysis of short-term and long-term salt-associated lncRNAs in the leaf of Avicennia marina.

As a highly salt-resistant mangrove, Avicennia marina can thrive in the hypersaline water. The leaves of Avicennia marina play a crucial role in salinity stress adaptability by secreting salt. Although the functions of long non-coding RNAs (lncRNAs) in leaves remain unknown, they have emerged as regulators in leaf development, aging and salt response. In this study, we employed transcriptomic data of both short-term and long-term salt treated leaves to identify salt-associated lncRNAs of leaf tissue. As a result, 687 short-term and 797 long-term salt-associated lncRNAs were identified. Notably, both short-term and long-term salt-associated lncRNAs exhibited slightly longer lengths and larger exons, but smaller introns compared with salt-non-associated lncRNAs. Furthermore, salt-associated lncRNAs also displayed higher tissue-specificity than salt-non-associated lncRNAs. Most of the salt-associated lncRNAs were common to short- and long-term salt treatments. And about one fifth of the downregulated salt-associated lncRNAs identified both in two terms were leaf tissue-specific lncRNAs. Besides, these leaf-specific lncRNAs were found to be involved in the oxidation-reduction and photosynthesis processes, as well as several metabolic processes, suggesting the noticeable functions of salt-associated lncRNAs in regulating salt responses of Avicennia marina leaves.

The evolution history of an allotetraploid mangrove tree analysed with a new tool Allo4D.

Mangrove species are broadly classified as true mangroves and mangrove associates. The latter are amphibious plants that can survive in the intertidal zone and reproduce naturally in terrestrial environments. Their widespread distribution and extensive adaptability make them ideal research materials for exploring adaptive evolution. In this study, we de novo assembled two genomes of mangrove associates (the allotetraploid Barringtonia racemosa (2n = 4x = 52) and diploid Barringtonia asiatica (2n = 2x = 26)) to investigate the role of allopolyploidy in the evolutionary history of mangrove species. We developed a new allotetraploid-dividing tool Allo4D to distinguish between allotetraploid scaffold-scale subgenomes and verified its accuracy and reliability using real and simulated data. According to the two subgenomes of allotetraploid B. racemosa divided using Allo4D, the allopolyploidization event was estimated to have occurred approximately one million years ago (Mya). We found that B. racemosa, B. asiatica, and Diospyros lotus shared a whole genome duplication (WGD) event during the K-Pg (Cretaceous-Paleozoic) period. K-Pg WGD and recent allopolyploidization events contributed to the speciation of B. racemosa and its adaptation to coastal habitats. We found that genes in the glucosinolates (GSLs) pathway, an essential pathway in response to various biotic and abiotic stresses, expanded rapidly in B. racemosa during polyploidization. In summary, this study provides a typical example of the adaptation of allopolyploid plants to extreme environmental conditions. The newly developed tool, Allo4D, can effectively divide allotetraploid subgenomes and explore the evolutionary history of polyploid plants, especially for species whose ancestors are unknown or extinct.

Metagenomic 16S rRNA analysis and predictive functional profiling revealed intrinsic organohalides respiration and bioremediation potential in mangrove sediment.

BACKGROUND: Mangrove sediment microbes are increasingly attracting scientific attention due to their demonstrated capacity for diverse bioremediation activities, encompassing a wide range of environmental contaminants. MATERIALS AND METHODS: The microbial communities of five Avicennia marina mangrove sediment samples collected from Al Rayyis White Head, Red Sea (KSA), were characterized using Illumina amplicon sequencing of the 16S rRNA genes. RESULTS: Our study investigated the microbial composition and potential for organohalide bioremediation in five mangrove sediments from the Red Sea. While Proteobacteria dominated four microbiomes, Bacteroidetes dominated the fifth. Given the environmental concerns surrounding organohalides, their bioremediation is crucial. Encouragingly, we identified phylogenetically diverse organohalide-respiring bacteria (OHRB) across all samples, including Dehalogenimonas, Dehalococcoides, Anaeromyxobacter, Desulfuromonas, Geobacter, Desulfomonile, Desulfovibrio, Shewanella and Desulfitobacterium. These bacteria are known for their ability to dechlorinate organohalides through reductive dehalogenation. PICRUSt analysis further supported this potential, predicting the presence of functional biomarkers for organohalide respiration (OHR), including reductive dehalogenases targeting tetrachloroethene (PCE) and 3-chloro-4-hydroxyphenylacetate in most sediments. Enrichment cultures studies confirmed this prediction, demonstrating PCE dechlorination by the resident microbial community. PICRUSt also revealed a dominance of anaerobic metabolic processes, suggesting the microbiome's adaptation to the oxygen-limited environment of the sediments. CONCLUSION: This study provided insights into the bacterial community composition of five mangrove sediments from the Red Sea. Notably, diverse OHRB were detected across all samples, which possess the metabolic potential for organohalide bioremediation through reductive dehalogenation pathways. Furthermore, PICRUSt analysis predicted the presence of functional biomarkers for OHR in most sediments, suggesting potential intrinsic OHR activity by the enclosed microbial community.

Metagenomic analysis of gut microbiome illuminates the mechanisms and evolution of lignocellulose degradation in mangrove herbivorous crabs.

BACKGROUND: Sesarmid crabs dominate mangrove habitats as the major primary consumers, which facilitates the trophic link and nutrient recycling in the ecosystem. Therefore, the adaptations and mechanisms of sesarmid crabs to herbivory are not only crucial to terrestrialization and its evolutionary success, but also to the healthy functioning of mangrove ecosystems. Although endogenous cellulase expressions were reported in crabs, it remains unknown if endogenous enzymes alone can complete the whole lignocellulolytic pathway, or if they also depend on the contribution from the intestinal microbiome. We attempt to investigate the role of gut symbiotic microbes of mangrove-feeding sesarmid crabs in plant digestion using a comparative metagenomic approach. RESULTS: Metagenomics analyses on 43 crab gut samples from 23 species of mangrove crabs with different dietary preferences revealed a wide coverage of 127 CAZy families and nine KOs targeting lignocellulose and their derivatives in all species analyzed, including predominantly carnivorous species, suggesting the crab gut microbiomes have lignocellulolytic capacity regardless of dietary preference. Microbial cellulase, hemicellulase and pectinase genes in herbivorous and detritivorous crabs were differentially more abundant when compared to omnivorous and carnivorous crabs, indicating the importance of gut symbionts in lignocellulose degradation and the enrichment of lignocellulolytic microbes in response to diet with higher lignocellulose content. Herbivorous and detritivorous crabs showed highly similar CAZyme composition despite dissimilarities in taxonomic profiles observed in both groups, suggesting a stronger selection force on gut microbiota by functional capacity than by taxonomy. The gut microbiota in herbivorous sesarmid crabs were also enriched with nitrogen reduction and fixation genes, implying possible roles of gut microbiota in supplementing nitrogen that is deficient in plant diet. CONCLUSIONS: Endosymbiotic microbes play an important role in lignocellulose degradation in most crab species. Their abundance is strongly correlated with dietary preference, and they are highly enriched in herbivorous sesarmids, thus enhancing their capacity in digesting mangrove leaves. Dietary preference is a stronger driver in determining the microbial CAZyme composition and taxonomic profile in the crab microbiome, resulting in functional redundancy of endosymbiotic microbes. Our results showed that crabs implement a mixed mode of digestion utilizing both endogenous and microbial enzymes in lignocellulose degradation, as observed in most of the more advanced herbivorous invertebrates.

Comparative analysis of gut microbiome of mangrove brachyuran crabs revealed patterns of phylosymbiosis and codiversification.

The acquisition of microbial symbionts enables animals to rapidly adapt to and exploit novel ecological niches, thus significantly enhancing the evolutionary fitness and success of their hosts. However, the dynamics of host-microbe interactions and their evolutionary implications remain largely underexplored in marine invertebrates. Crabs of the family Sesarmidae (Crustacea: Brachyura) are dominant inhabitants of mangrove forests and are considered keystone species there. Their rapid diversification, particularly after adopting a plant-feeding lifestyle, is believed to have been facilitated by symbiotic gut microbes, enabling successful colonization of intertidal and terrestrial environments. To investigate the patterns and mechanisms shaping the microbial communities and the role of microbes in the evolution of Sesarmidae, we characterized and compared the gut microbiome compositions across 43 crab species from Sesarmidae and other mangrove-associated families using 16S metabarcoding. We found that the gut microbiome assemblages in crabs are primarily determined by host identity, with a secondary influence from environmental factors such as microhabitat and sampling location, and to a lesser extent influenced by biological factors such as sex and gut region. While patterns of phylosymbiosis (i.e. when microbial community relationships recapitulate the phylogeny of their hosts) were consistently observed in all beta-diversity metrics analysed, the strength of phylosymbiosis varied across crab families. This suggests that the bacterial assemblages in each family were differentially shaped by different degrees of host filtering and/or other evolutionary processes. Notably, Sesarmidae displayed signals of cophylogeny with its core gut bacterial genera, which likely play crucial functional roles in their hosts by providing lignocellulolytic enzymes, essential amino acids, and fatty acids supplementation. Our results support the hypothesis of microbial contribution to herbivory and terrestrialization in mangrove crabs, highlighting the tight association and codiversification of the crab holobiont.

Brassinosteroid enhances salt tolerance via S-nitrosoglutathione reductase and nitric oxide signaling pathway in mangrove Kandelia obovata.

Brassinosteroid (BR) has been shown to modulate plant tolerance to various stresses. S-nitrosoglutathione reductase (GSNOR) is involved in the plant response to environment stress by fine-turning the level of nitric oxide (NO). However, whether GSNOR is involved in BR-regulated Na+ /K+ homeostasis to improve the salt tolerance in halophyte is unknown. Here, we firstly reported that high salinity increases the expression of BR-biosynthesis genes and the endogenous levels of BR in mangrove Kandelia obovata. Then, salt-induced BR triggers the activities and gene expressions of GSNOR and antioxidant enzymes, thereafter decrease the levels of malondialdehyde, hydrogen peroxide. Subsequently, BR-mediated GSNOR negatively regulates NO contributions to the reduction of reactive oxygen species generation and induction of the gene expression related to Na+ and K+ transport, leading to the decrease of Na+ /K+ ratio in the roots of K. obovata. Finally, the applications of exogenous BR, NO scavenger, BR biosynthetic inhibitor and GSNOR inhibitor further confirm the function of BR. Taken together, our result provides insight into the mechanism of BR in the response of mangrove K. obovata to high salinity via GSNOR and NO signaling pathway by reducing oxidative damage and modulating Na+ /K+ homeostasis.

Genome-wide identification of Avicennia marina aquaporins reveals their role in adaptation to intertidal habitats and their relevance to salt secretion and vivipary.

Aquaporins (AQPs) regulate the transport of water and other substrates, aiding plants in adapting to stressful environments. However, the knowledge of AQPs in salt-secreting and viviparous Avicennia marina is limited. In this study, 46 AmAQPs were identified in A. marina genome, and their subcellular localisation and function in transporting H2 O2 and boron were assessed through bioinformatics analysis and yeast transformation. Through analysing their expression patterns via RNAseq and real-time quantitative polymerase chain reaction, we found that most AmAQPs were downregulated in response to salt and tidal flooding. AmPIP (1;1, 1;7, 2;8, 2;9) and AmTIP (1;5, 1;6) as salt-tolerant candidate genes may contribute to salt secretion together with Na+ /H+ antiporters. AmPIP2;1 and AmTIP1;5 were upregulated during tidal flooding and may be regulated by anaerobic-responsive element and ethylene-responsive element cis-elements, aiding in adaptation to tidal inundation. Additionally, we found that the loss of the seed desiccation and dormancy-related TIP3 gene, and the loss of the seed dormancy regulator DOG1 gene, or DOG1 protein lack heme-binding capacity, may be genetic factors contributing to vivipary. Our findings shed light on the role of AQPs in A. marina adaptation to intertidal environments and their relevance to salt secretion and vivipary.

PlantC2U: deep learning of cross-species sequence landscapes predicts plastid C-to-U RNA editing in plants.

In plants, C-to-U RNA editing mainly occurs in plastid and mitochondrial transcripts, which contributes to a complex transcriptional regulatory network. More evidence reveals that RNA editing plays critical roles in plant growth and development. However, accurate detection of RNA editing sites using transcriptome sequencing data alone is still challenging. In the present study, we develop PlantC2U, which is a convolutional neural network, to predict plastid C-to-U RNA editing based on the genomic sequence. PlantC2U achieves >95% sensitivity and 99% specificity, which outperforms the PREPACT tool, random forests, and support vector machines. PlantC2U not only further checks RNA editing sites from transcriptome data to reduce possible false positives, but also assesses the effect of different mutations on C-to-U RNA editing based on the flanking sequences. Moreover, we found the patterns of tissue-specific RNA editing in the mangrove plant Kandelia obovata, and observed reduced C-to-U RNA editing rates in the cold stress response of K. obovata, suggesting their potential regulatory roles in plant stress adaptation. In addition, we present RNAeditDB, available online at https://jasonxu.shinyapps.io/RNAeditDB/. Together, PlantC2U and RNAeditDB will help researchers explore the RNA editing events in plants and thus will be of broad utility for the plant research community.

Functional composition outweighs taxonomic and functional diversity in maintaining ecosystem properties and processes of mangrove forests.

Biodiversity loss can have significant consequences for human well-being, as it can affect multiple ecosystem properties and processes (MEPP) that drive ecosystem services. However, a comprehensive understanding of the link between environmental factors, biodiversity, and MEPP remains elusive, especially in mangrove ecosystems that millions of people along tropical coastlines worldwide depend upon. Here, we collated a comprehensive dataset on forest inventory, plant traits, and environmental factors across 93 plots in the Sundarbans Reserved Forests, Bangladesh. The functional composition (FC) of leaf area showed a stronger positive association with MEPP, being determined by total biomass and productivity of the mangroves, sediment organic carbon, and ammonium, phosphorus, and potassium contents of the sediment, than species richness (SR) or functional diversity (FD). Further, FC mediated a strong negative association of sediment salinity, and a positive association of SR, with MEPP. The similar but opposite total associations of SR and sediment salinity with MEPP suggest that species-rich mangroves could offset the negative impacts of rising salinity on MEPP. When focusing on a single aspect of MEPP, both FD and FC mattered, with the FD of leaf area showing a strong association with mangrove productivity and sediment potassium content, while the FC of leaf litter nitrogen showed the strongest associations with sediment ammonium and phosphorus contents. Therefore, to sustain mangrove ecosystems as a reliable nature-based solution for climate change mitigation, conservation and (re-)establishment projects should prioritize regionally dominant species with high leaf area and nitrogen content, plus functionally different species to support the ecosystem processes and services provided by mangroves.

Blue carbon sink capacity of mangroves determined by leaves and their associated microbiome.

Mangroves play a globally significant role in carbon capture and storage, known as blue carbon ecosystems. Yet, there are fundamental biogeochemical processes of mangrove blue carbon formation that are inadequately understood, such as the mechanisms by which mangrove afforestation regulates the microbial-driven transfer of carbon from leaf to below-ground blue carbon pool. In this study, we addressed this knowledge gap by investigating: (1) the mangrove leaf characteristics using state-of-the-art FT-ICR-MS; (2) the microbial biomass and their transformation patterns of assimilated plant-carbon; and (3) the degradation potentials of plant-derived carbon in soils of an introduced (Sonneratia apetala) and a native mangrove (Kandelia obovata). We found that biogeochemical cycling took entirely different pathways for S. apetala and K. obovata. Blue carbon accumulation and the proportion of plant-carbon for native mangroves were high, with microbes (dominated by K-strategists) allocating the assimilated-carbon to starch and sucrose metabolism. Conversely, microbes with S. apetala adopted an r-strategy and increased protein- and nucleotide-biosynthetic potentials. These divergent biogeochemical pathways were related to leaf characteristics, with S. apetala leaves characterized by lower molecular-weight, C:N ratio, and lignin content than K. obovata. Moreover, anaerobic-degradation potentials for lignin were high in old-aged soils, but the overall degradation potentials of plant carbon were age-independent, explaining that S. apetala age had no significant influences on the contribution of plant-carbon to blue carbon. We propose that for introduced mangroves, newly fallen leaves release nutrient-rich organic matter that favors growth of r-strategists, which rapidly consume carbon to fuel growth, increasing the proportion of microbial-carbon to blue carbon. In contrast, lignin-rich native mangrove leaves shape K-strategist-dominated microbial communities, which grow slowly and store assimilated-carbon in cells, ultimately promoting the contribution of plant-carbon to the remarkable accumulation of blue carbon. Our study provides new insights into the molecular mechanisms of microbial community responses during reforestation in mangrove ecosystems.

Saccharopolyspora mangrovi sp. nov., a novel mangrove soil actinobacterium with distinct metabolic potential revealed by comparative genomic analysis.

A novel mangrove soil-derived actinomycete, strain S2-29T, was found to be most closely related to Saccharopolyspora karakumensis 5K548T based on 16 S rRNA sequence (99.24% similarity) and genomic phylogenetic analyses. However, significant divergence in digital DNA-DNA hybridization, average nucleotide identity, and unique biosynthetic gene cluster possession distinguished S2-29T as a distinct Saccharopolyspora species. Pan genome evaluation revealed exceptional genomic flexibility in genus Saccharopolyspora, with > 95% accessory genome content. Strain S2-29T harbored 718 unique genes, largely implicated in energetic metabolisms, indicating different metabolic capacities from its close relatives. Several uncharacterized biosynthetic gene clusters in strain S2-29T highlighted the strain's untapped capacity to produce novel functional compounds with potential biotechnological applications. Designation as novel species Saccharopolyspora mangrovi sp. nov. (type strain S2-29T = JCM 34,548T = CGMCC 4.7716T) was warranted, expanding the known Saccharopolyspora diversity and ecology. The discovery of this mangrove-adapted strain advances understanding of the genus while highlighting an untapped source of chemical diversity.

Diversity, distribution, and bioprospecting potentials of carotenogenic yeast from mangrove ecosystem.

Microbial production of carotenoids has gained significant interest for its cost-effectiveness and sustainable nature. This study focuses on 47 red-pigmented yeasts isolated from sediments and plant parts of 13 species of mangrove trees. The relative abundance and distribution of these yeasts varied with plant species and plant parts. The highest number of red yeasts was associated with the mangrove plant Avicennia officinalis (32%). Notably, the leaves harbored the highest percentage (45%) of carotenogenic yeasts, and definite compartmentalization of these yeast species was noticed in mangrove plant parts. All the isolates were molecularly identified and they belonged to the genera of Rhodotorula, Rhodosporidiobolus, and Cryptococcus. The diversity of the pigmented yeasts isolated from A. officinalis was found to be the greatest. Among these strains, Rhodotorula mucilaginosa PV 8 was identified as the most potent producer of carotenoid pigment. Under optimized conditions of physical parameters - 28 °C, pH 5, and 15% salinity led to biomass production of 9.2 ± 0.12 g/L DCW and a pigment yield of 194.78 µg/g. The pigment produced by PV 8 was identified as ß-carotene by thin layer chromatography (TLC) and Fourier transform infrared spectroscopy (FT-IR). This ß-carotene demonstrated strong antioxidant activity. Moreover, the carotenoid displayed promising antibacterial activity against multidrug-resistant organisms, including Aeromonas sp. and Vibrio sp. In vitro studies revealed the probiotic traits of PV 8. The cytotoxicity of R. mucilaginosa PV 8 was assessed in the invertebrate model Artemia salina and the survival rate showed that it was non-toxic. Furthermore, the ß-carotene from PV 8 demonstrated the ability to transfer its vibrant color to various food products, maintaining color stability even under varied conditions. This research underscores the potential of R. mucilaginosa PV 8, as a versatile and valuable resource for the production of carotenoids.