ORCID Profile
0000-0002-7616-3637
Current Organisation
San Diego State University Research Foundation
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Publisher: Research Square Platform LLC
Date: 15-06-2021
DOI: 10.21203/RS.3.RS-600995/V1
Abstract: Background The coral holobiont is comprised of a highly erse microbial community that provides key services to corals such as protection against pathogens and nutrient cycling. The coral surface mucus layer (SML) microbiome is very sensitive to external changes and tied to ecosystem functioning, as it constitutes the direct interface between the coral host and the environment. The functional profile of microbial genes in the coral SML is underexplored and the use of shotgun metagenomics is relatively rare among coral microbiome studies. Here we investigate whether the bacterial taxonomic and functional profiles in the coral SML are shaped by the local reef zone and explore their role in coral health and ecosystem functioning. Results The analysis was conducted using metagenomes and metagenome assemble genomes (MAGs) associated with the coral Pseudodiploria strigosa and the water column from two naturally distinct reef environments in Bermuda: inner patch reefs exposed to a fluctuating thermal regime and the more stable outer reefs . Our results showed that the microbial community structure is simultaneously selected by the host medium (i.e., coral SML versus water) and the local environment (i.e., inner reefs versus outer reefs), both at taxonomic and functional levels. The coral SML microbiome from inner reefs provides more gene functions that are involved in nutrient cycling (e.g., photosynthesis, phosphorus metabolism, sulfur assimilation) and that are related to higher levels of microbial activity, competition, and stress response, such as dimethylsulfoniopropionate (DMSP) breakdown. In contrast, the coral SML microbiome from outer reefs contained genes indicative of a carbohydrate-rich mucus composition found in corals exposed to less stressful temperatures and showed high proportions of microbial gene functions that play a potential role in coral disease, such as degradation of lignin-derived compounds and sulfur oxidation. Conclusion The fluctuating environment in the inner patch reefs of Bermuda could be driving a more beneficial coral SML microbiome potentially increasing holobiont resilience to environmental changes and disease. Our results reveal microbial taxa and functions selected at reef scale in the coral SML microbiome that can leverage disease management, microbiome engineering, and microbial eco-evolutionary theories.
Publisher: American Society for Microbiology
Date: 28-04-2020
Abstract: Coral microbiome dysbiosis (i.e., shifts in the microbial community structure or complete loss of microbial symbionts) caused by environmental changes is a key player in the decline of coral health worldwide. Multiple factors in the water column and the surrounding biological community influence the dynamics of the coral microbiome. However, by including only temperature as an external factor, our model proved to be successful in describing the microbial community associated with the surface mucus layer (SML) of the coral P. strigosa . The dynamic model developed and validated in this study is a potential tool to predict the coral microbiome under different temperature conditions.
Publisher: MDPI AG
Date: 21-10-2022
DOI: 10.3390/MICROORGANISMS10102081
Abstract: Characterizations of shark-microbe systems in wild environments have outlined patterns of species-specific microbiomes however, whether captivity affects these trends has yet to be determined. We used high-throughput shotgun sequencing to assess the epidermal microbiome belonging to leopard sharks (Triakis semifasciata) in captive (Birch Aquarium, La Jolla California born and held permanently in captivity), semi-captive (held in captivity for year in duration and scheduled for release Scripps Institute of Oceanography, San Diego, CA, USA) and wild environments (Moss Landing and La Jolla, CA, USA). Here, we report captive environments do not drive epidermal microbiome compositions of T. semifasciata to significantly erge from wild counterparts as life-long captive sharks maintain a species-specific epidermal microbiome resembling those associated with semi-captive and wild populations. Major taxonomic composition shifts observed were inverse changes of top taxonomic contributors across captive duration, specifically an increase of Pseudoalteromonadaceae and consequent decrease of Pseudomonadaceae relative abundance as T. semifasciata increased duration in captive conditions. Moreover, we show captivity did not lead to significant losses in microbial α- ersity of shark epidermal communities. Finally, we present a novel association between T. semifasciata and the Muricauda genus as Metagenomes associated genomes revealed a consistent relationship across captive, semi-captive, and wild populations. Since changes in microbial communities is often associated with poor health outcomes, our report illustrates that epidermally associated microbes belonging to T. semifasciata are not suffering detrimental impacts from long or short-term captivity. Therefore, conservation programs which house sharks in aquariums are providing a healthy environment for the organisms on display. Our findings also expand on current understanding of shark epidermal microbiomes, explore the effects of ecologically different scenarios on benthic shark microbe associations, and highlight novel associations that are consistent across captive gradients.
Publisher: Springer Science and Business Media LLC
Date: 13-06-2020
DOI: 10.1186/S40168-020-00840-X
Abstract: The vertebrate clade erged into Chondrichthyes (sharks, rays, and chimeras) and Osteichthyes fishes (bony fishes) approximately 420 mya, with each group accumulating vast anatomical and physiological differences, including skin properties. The skin of Chondrichthyes fishes is covered in dermal denticles, whereas Osteichthyes fishes are covered in scales and are mucous rich. The ergence time among these two fish groups is hypothesized to result in predictable variation among symbionts. Here, using shotgun metagenomics, we test if patterns of ersity in the skin surface microbiome across the two fish clades match predictions made by phylosymbiosis theory. We hypothesize (1) the skin microbiome will be host and clade-specific, (2) evolutionary difference in elasmobranch and teleost will correspond with a concomitant increase in host-microbiome dissimilarity, and (3) the skin structure of the two groups will affect the taxonomic and functional composition of the microbiomes. We show that the taxonomic and functional composition of the microbiomes is host-specific. Teleost fish had lower average microbiome within clade similarity compared to among clade comparison, but their composition is not different among clade in a null based model. Elasmobranch’s average similarity within clade was not different than across clade and not different in a null based model of comparison. In the comparison of host distance with microbiome distance, we found that the taxonomic composition of the microbiome was related to host distance for the elasmobranchs, but not the teleost fishes. In comparison, the gene function composition was not related to the host-organism distance for elasmobranchs but was negatively correlated with host distance for teleost fishes. Our results show the patterns of phylosymbiosis are not consistent across both fish clades, with the elasmobranchs showing phylosymbiosis, while the teleost fish are not. The discrepancy may be linked to alternative processes underpinning microbiome assemblage, including possible historical host-microbiome evolution of the elasmobranchs and convergent evolution in the teleost which filter specific microbial groups. Our comparison of the microbiomes among fishes represents an investigation into the microbial relationships of the oldest ergence of extant vertebrate hosts and reveals that microbial relationships are not consistent across evolutionary timescales.
Publisher: Frontiers Media SA
Date: 16-08-2022
DOI: 10.3389/FMARS.2022.908734
Abstract: Caribbean reefs have undergone large-scale losses in coral cover in past decades, sparking a search for species that are resilient under stress. Porites astreoides has been considered a “winner” and a key player in sustaining coral cover in the Caribbean as more sensitive species struggle. However, P. astreoides has recently declined in abundance, raising concern about its status as a winner. Here, we reviewed the ecophysiology of P. astreoides in response to environmental stress to elucidate whether this species could thrive in the future of Caribbean reefs. We examined ecophysiological variables of P. astreoides related to photosynthesis, growth, recruitment, tissue condition, and microbiome in response to temperature, pH, macroalgal competition, depth, and sedimentation. Overall, P. astreoides was sensitive to environmental stress and each physiological feature showed varying levels of sensitivity. Coral-algal photosynthesis and coral tissue condition could withstand single events of thermal stress but reflected a metabolic imbalance that hinders recovery from repeated bleaching events, compromising long-term success. Colony growth was particularly vulnerable to low pH and macroalgal competition. Recruitment was unaffected, or even favored, by depth and could tolerate high temperatures, but it was sensitive to exposure to macroalgae, especially in combination with abiotic stressors. The response of the microbiome of P. astreoides to stressors is still poorly understood. In relation to other corals, P. astreoides was frequently reported as the most sensitive species in the reviewed literature. The success of P. astreoides is tightly integrated into the future of Caribbean reefs, which could be losing an old winner.
Publisher: MDPI AG
Date: 05-09-2022
DOI: 10.3390/V14091969
Abstract: The epidermal microbiome is a critical element of marine organismal immunity, but the epidermal virome of marine organisms remains largely unexplored. The epidermis of sharks represents a unique viromic ecosystem. Sharks secrete a thin layer of mucus which harbors a erse microbiome, while their hydrodynamic dermal denticles simultaneously repel environmental microbes. Here, we s led the virome from the epidermis of three shark species in the family Carcharhinidae: the genetically and morphologically similar Carcharhinus obscurus (n = 6) and Carcharhinus galapagensis (n = 10) and the outgroup Galeocerdo cuvier (n = 15). Virome taxonomy was characterized using shotgun metagenomics and compared with a suite of multivariate analyses. All three sharks retain species-specific but highly similar epidermal viromes dominated by uncharacterized bacteriophages which vary slightly in proportional abundance within and among shark species. Intraspecific variation was lower among C. galapagensis than among C. obscurus and G. cuvier. Using both the annotated and unannotated reads, we were able to determine that the Carcharhinus galapagensis viromes were more similar to that of G. cuvier than they were to that of C. obscurus, suggesting that behavioral niche may be a more prominent driver of virome than host phylogeny.
Publisher: Authorea, Inc.
Date: 03-02-2023
DOI: 10.22541/AU.167542930.03517639/V1
Abstract: Coral reef health is tightly connected to the coral microbiome. Coral bleaching and disease outbreaks have caused an unprecedented loss in coral cover worldwide, particularly correlated to a warming ocean. Coping mechanisms of the coral holobiont under high temperatures are not completely described, but the associated microbial community is a potential source of acquired heat-tolerance. The relationship between stress and stability in the microbiome is key to understanding the role that the coral microbiome plays in thermal tolerance. According to the Anna Karenina Principle (AKP), stress or disease will increase instability and stochasticity among animal microbiomes. Here we investigate whether heat stress results in microbiomes that follow the AKP. We used shotgun metagenomics in an experimental setting to understand the dynamics of microbial taxa and genes in the surface mucous layer (SML) microbiome of the coral Pseudodiploria strigosa under heat treatment. The metagenomes of corals exposed to heat stress showed high similarity, indicating a deterministic and stable response of the coral microbiome to disturbance, in opposition to the AKP. We hypothesize that this stability is the result of a selective pressure towards a coral microbiome that is assisting the holobiont to withstand heat stress. The coral SML microbiome responded to heat stress with an increase in the relative abundance of taxa with probiotic potential, and functional genes for nitrogen and sulfur acquisition. These consistent and specific microbial taxa and gene functions that significantly increased in proportional abundance in corals exposed to heat are potentially beneficial to coral health and thermal resistance.
Publisher: Springer Science and Business Media LLC
Date: 15-08-2023
DOI: 10.1007/S00248-022-02094-6
Abstract: The coral holobiont is comprised of a highly erse microbial community that provides key services to corals such as protection against pathogens and nutrient cycling. The coral surface mucus layer (SML) microbiome is very sensitive to external changes, as it constitutes the direct interface between the coral host and the environment. Here, we investigate whether the bacterial taxonomic and functional profiles in the coral SML are shaped by the local reef zone and explore their role in coral health and ecosystem functioning. The analysis was conducted using metagenomes and metagenome-assembled genomes (MAGs) associated with the coral Pseudodiploria strigosa and the water column from two naturally distinct reef environments in Bermuda: inner patch reefs exposed to a fluctuating thermal regime and the more stable outer reefs. The microbial community structure in the coral SML varied according to the local environment, both at taxonomic and functional levels. The coral SML microbiome from inner reefs provides more gene functions that are involved in nutrient cycling (e.g., photosynthesis, phosphorus metabolism, sulfur assimilation) and those that are related to higher levels of microbial activity, competition, and stress response. In contrast, the coral SML microbiome from outer reefs contained genes indicative of a carbohydrate-rich mucus composition found in corals exposed to less stressful temperatures and showed high proportions of microbial gene functions that play a potential role in coral disease, such as degradation of lignin-derived compounds and sulfur oxidation. The fluctuating environment in the inner patch reefs of Bermuda could be driving a more beneficial coral SML microbiome, potentially increasing holobiont resilience to environmental changes and disease.
Publisher: Springer Science and Business Media LLC
Date: 07-02-2022
DOI: 10.1007/S00248-022-01969-Y
Abstract: The epidermis of Chondrichthyan fishes consists of dermal denticles with production of minimal but protein-rich mucus that collectively, influence the attachment and biofilm development of microbes, facilitating a unique epidermal microbiome. Here, we use metagenomics to provide the taxonomic and functional characterization of the epidermal microbiome of the Triakis semifasciata (leopard shark) at three time-points collected across 4 years to identify links between microbial groups and host metabolism. Our aims include (1) describing the variation of microbiome taxa over time and identifying recurrent microbiome members (present across all time-points) (2) investigating the relationship between the recurrent and flexible taxa (those which are not found consistently across time-points) (3) describing the functional compositions of the microbiome which may suggest links with the host metabolism and (4) identifying whether metabolic processes are shared across microbial genera or are unique to specific taxa. Microbial members of the microbiome showed high similarity between all in iduals (Bray-Curtis similarity index = 82.7, where 0 = no overlap, 100 = total overlap) with the relative abundance of those members varying across s ling time-points, suggesting flexibility of taxa in the microbiome. One hundred and eighty-eight genera were identified as recurrent, including Pseudomonas, Erythrobacter, Alcanivorax, Marinobacter, and Sphingopxis being consistently abundant across time-points, while Limnobacter and Xyella exhibited switching patterns with high relative abundance in 2013, Sphingobium and Sphingomona in 2015, and Altermonas, Leeuwenhoekiella, Gramella, and Maribacter in 2017. Of the 188 genera identified as recurrent, the top 19 relatively abundant genera formed three recurrent groups. The microbiome also displayed high functional similarity between in iduals (Bray-Curtis similarity index = 97.6) with gene function composition remaining consistent across all time-points. These results show that while the presence of microbial genera exhibits consistency across time-points, their abundances do fluctuate. Microbial functions however remain stable across time-points thus, we suggest the leopard shark microbiomes exhibit functional redundancy. We show coexistence of microbes hosted in elasmobranch microbiomes that encode genes involved in utilizing nitrogen, but not fixing nitrogen, degrading urea, and resistant to heavy metal.
Publisher: Cold Spring Harbor Laboratory
Date: 16-05-2022
DOI: 10.1101/2022.05.15.492003
Abstract: Analysis of viral ersity using modern sequencing technologies offers extraordinary opportunities for discovery. However, these analyses present a number of bioinformatic challenges due to viral genetic ersity and virome complexity. Due to the lack of conserved marker sequences, metagenomic detection of viral sequences requires a non-targeted, random (shotgun) approach. Annotation and enumeration of viral sequences relies on rigorous quality control and effective search strategies against appropriate reference databases. Virome analysis also benefits from the analysis of both in idual metagenomic sequences as well as assembled contigs. Combined, virome analysis results in large amounts of data requiring sophisticated visualization and statistical tools. Here we introduce Hecatomb, a bioinformatics platform enabling both read and contig based analysis. Hecatomb integrates query information from both amino acid and nucleotide reference sequence databases. Hecatomb integrates data collected throughout the workflow enabling analyst driven virome analysis and discovery. Hecatomb is available on GitHub at handley/hecatomb . Hecatomb provides a single, modular software solution to the complex tasks required of many virome analysis. We demonstrate the value of the approach by applying Hecatomb to both a host-associated (enteric) and an environmental (marine) virome data set. Hecatomb provided data to determine true- or false-positive viral sequences in both data sets and revealed complex virome structure at distinct marine reef sites.
Publisher: Frontiers Media SA
Date: 02-03-2023
DOI: 10.3389/FMICB.2023.1031711
Abstract: Marine host-associated microbiomes are affected by a combination of species-specific (e.g., host ancestry, genotype) and habitat-specific features (e.g., environmental physiochemistry and microbial biogeography). The stingray epidermis provides a gradient of characteristics from high dermal denticles coverage with low mucus to reduce dermal denticles and high levels of mucus. Here we investigate the effects of host phylogeny and habitat by comparing the epidermal microbiomes of Myliobatis californica (bat rays) with a mucus rich epidermis, and Urobatis halleri (round rays) with a mucus reduced epidermis from two locations, Los Angeles and San Diego, California (a 150 km distance). We found that host microbiomes are species-specific and distinct from the water column, however composition of M. californica microbiomes showed more variability between in iduals compared to U. halleri. The variability in the microbiome of M. californica caused the microbial taxa to be similar across locations, while U. halleri microbiomes were distinct across locations. Despite taxonomic differences, Shannon ersity is the same across the two locations in U. halleri microbiomes suggesting the taxonomic composition are locally adapted, but ersity is maintained by the host. Myliobatis californica and U. halleri microbiomes maintain functional similarity across Los Angeles and San Diego and each ray showed several unique functional genes. Myliobatis californica has a greater relative abundance of RNA Polymerase III-like genes in the microbiome than U. halleri , suggesting specific adaptations to a heavy mucus environment. Construction of Metagenome Assembled Genomes (MAGs) identified novel microbial species within Rhodobacteraceae , Moraxellaceae , Caulobacteraceae , Alcanivoracaceae and Gammaproteobacteria. All MAGs had a high abundance of active RNA processing genes, heavy metal, and antibiotic resistant genes, suggesting the stingray mucus supports high microbial growth rates, which may drive high levels of competition within the microbiomes increasing the antimicrobial properties of the microbes.
Location: United States of America
No related grants have been discovered for Laís Farias Oliveira Lima.