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Comparative Metagenomic Analysis of Biosynthetic Diversity across Sponge Microbiomes Highlights Metabolic Novelty, Conservation, and Diversification

Marine sponges and their microbial symbiotic communities are rich sources of diverse natural products (NPs) that often display biological activity, yet little is known about the global distribution of NPs and the symbionts that produce them. Since the majority of sponge symbionts remain uncultured, it is a challenge to characterize their NP biosynthetic pathways, assess their prevalence within the holobiont, and measure the diversity of NP biosynthetic gene clusters (BGCs) across sponge taxa and environments. Here, we explore the microbial biosynthetic landscapes of three high-microbial-abundance (HMA) sponges from the Atlantic Ocean and the Mediterranean Sea. This data set reveals striking novelty, with <1% of the recovered gene cluster families (GCFs) showing similarity to any characterized BGC. When zooming in on the microbial communities of each sponge, we observed higher variability of specialized metabolic and taxonomic profiles between sponge species than within species. Nonetheless, we identified conservation of GCFs, with 20% of sponge GCFs being shared between at least two sponge species and a GCF core comprised of 6% of GCFs shared across all species. Within this functional core, we identified a set of widespread and diverse GCFs encoding nonribosomal peptide synthetases that are potentially involved in the production of diversified ether lipids, as well as GCFs putatively encoding the production of highly modified proteusins. The present work contributes to the small, yet growing body of data characterizing NP landscapes of marine sponge symbionts and to the cryptic biosynthetic potential contained in this environmental niche.

Catarina Loureiro, Anastasia Galani, Asimenia Gavriilidou, etc.

Research Article, Facultad de ciencias de la Universidad Nacional Sede Bogotá, (2022)

Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus *Amanita*

Fungi are evolutionary shape shifters and adapt quickly to new environments. Ectomycorrhizal (EM) symbioses are mutualistic associations between fungi and plants and have evolved repeatedly and independently across the fungal tree of life, suggesting lineages frequently reconfigure genome content to take advantage of open ecological niches. To date analyses of genomic mechanisms facilitating EM symbioses have involved comparisons of distantly related species, but here, we use the genomes of three EM and two asymbiotic (AS) fungi from the genus Amanita as well as an AS outgroup to study genome evolution following a single origin of symbiosis. Our aim was to identify the defining features of EM genomes, but our analyses suggest no clear differentiation of genome size, gene repertoire size, or transposable element content between EM and AS species.

Jaqueline Hess, Inger Skrede, Maryam Chaib De Mares, Matthieu Hainaut, Bernard Henrissat, Anne Pringle

Research Article, Facultad de ciencias de la Universidad Nacional Sede Bogotá, (2022)

Lista de publicaciones

Grupo de Investigación (BMTE)

“Distinct bacteria display genus and species-specific associations with mycobionts in paramo lichens in Colombia”.
M. C. D. Mares et al.
Oxford Academic, 2025
ABS BIB

Lichens are complex symbiotic systems where fungi interact with an extracellular arrangement of one or more photosynthetic partners and an indeterminate number of other microbes. Recently, specific lichen–microbial community associations have been proposed. In this study, we aimed to characterize the differences in bacteria associated with closely related lichens, under a defined set of environmental conditions in Colombian paramos. Our goal was to determine if there is a correlation between microbiota and host divergence in lichen species belonging to the genus Sticta. We found that specific microbiota are defined by their mycobiont at the genus level. Further, distinct bacterial families show differences among the three studied genera, and specific amplicon sequence variants further discriminate among lichen species within each genus. A geographic component also determines the composition of these microbial communities among lichen species. Our functional analysis revealed that fungal partners play a key role in synthesizing complex polysaccharides, while bacterial-derived antioxidants and photoprotective mechanisms contribute to desiccation tolerance in lichens. These insights highlight the complex interactions within lichen symbioses that could be relevant in environments such as the paramo ecosystem.
@article{GRL5_Mares_Chaib_2025, title = {Distinct bacteria display genus and species-specific associations with mycobionts in paramo lichens in Colombia}, journal = {Oxford Academic}, author = {Mares, Maryam Chaib De and Castro, Emerson Arciniegas and Ulloa, Maria Alejandra and Torres, Jean Marc and Sierra, Maria A and Butler, Daniel J and Mason, Christopher E and Zambrano, María Mercedes and Moncada, Bibiana and Muñoz, Alejandro Reyes}, year = {2025}, doi = {10.1093/femsec/fiaf010}, image_filename = {}, published = {1}, tag = {10001} }
“Expressed protein profile of a Tectomicrobium and other microbial symbionts in the marine sponge Aplysina aerophoba as evidenced by metaproteomics”.
M. C. D. Mares et al.
Nature, 2018
ABS BIB

Aplysina aerophoba is an emerging model marine sponge, with a well-characterized microbial community in terms of diversity and structure. However, little is known about the expressed functional capabilities of its associated microbes. Here, we present the first metaproteomics-based study of the microbiome of A. aerophoba. We found that transport and degradation of halogenated and chloroaromatic compounds are common active processes in the sponge microbiomes
@article{GRL1_Mares_Chaib2018, title = {Expressed protein profile of a Tectomicrobium and other microbial symbionts in the marine sponge Aplysina aerophoba as evidenced by metaproteomics}, journal = {Nature}, author = {Mares, Maryam Chaib De and Jiménez, Diego Javier and Palladino, Giorgia and Gutleben, Johanna and Lebrun, Laura A. and Muller, Emilie E. L. and Wilmes, Paul and Sipkema, Detmer and van Elsas, Jan Dirk}, year = {2018}, doi = {10.1038/s41598-018-30134-0}, image_filename = {./images/publications/GRL1_Mares_Chaib2018.webp}, published = {1}, tag = {10001} }
“Evidence for human microRNA-offset RNAs in small RNA sequencing data”.
D. Langenberger, C. Bermudez-Santana, J. Hertel, S. Hoffmann, P. Khaitovich, and P. F. Stadler.
Oxford University Press, 2009
ABS BIB

MicroRNA-offset-RNAs (moRNAs) were recently detected as highly abundant class of small RNAs in a basal chordate. Using short read sequencing data, we show here that moRNAs are also produced from human microRNA precursors, albeit at quite low expression levels. The expression levels of moRNAs are unrelated to those of the associated microRNAs. Surprisingly, microRNA precursors that also show moRNAs are typically evolutionarily old, comprising more than half of the microRNA families that were present in early Bilateria, while evidence for moRNAs was found only for a relative small fraction of microRNA families of recent origin.
@article{GRL2_Langenberger_David2009, title = {Evidence for human microRNA-offset RNAs in small RNA sequencing data}, journal = {Oxford University Press}, author = {Langenberger, David and Bermudez-Santana, Clara and Hertel, Jana and Hoffmann, Steve and Khaitovich, Philipp and Stadler, Peter F.}, year = {2009}, doi = {10.1093/bioinformatics/btp419}, image_filename = {./images/publications/GRL2_Langenberger_David2009.png}, published = {1}, tag = {10002} }
“Design of gene circuits in microorganisms to modulate host physiology”.
E. B. Gomez, J. C. Naranjo, L. M. R. Loaiza, C. Vega, J. C. R. Medina, and F. Gomez.
Sociedad Colombiana de Ciencias Químicas, 2023
ABS BIB

This paper recapitulates a brief history of the emergence and definition of synthetic biology, summarizes the basic concepts to understand how it is practiced, describes how it articulates with industry in terms of innovation, and introduces the most recent applications of artificial intelligence in this area.
@article{GRL4_Mares_Chaib2023, title = {Design of gene circuits in microorganisms to modulate host physiology}, journal = {Sociedad Colombiana de Ciencias Químicas}, author = {Gomez, Edgar Babativa and Naranjo, Julieth Camila and Loaiza, Luis Miguel Riveros and Vega, Catalina and Medina, Juan Carlos Riveros and Gomez, Francisco}, year = {2023}, image_filename = {./images/publications/GRL4_Mares_Chaib2023.png}, published = {1}, tag = {10003} }
“Horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal Amanita”.
M. C. D. Mares et al.
New Phytologist Foundation, 2014
ABS BIB

The genus Amanita encompasses both symbiotic, ectomycorrhizal fungi and asymbiotic litter decomposers; all species are derived from asymbiotic ancestors. Symbiotic species are no longer able to degrade plant cell walls. The carbohydrate esterases family 1 (CE1s) is a diverse group of enzymes involved in carbon metabolism, including decomposition and carbon storage. CE1 genes of the ectomycorrhizal A. muscaria appear diverged from all other fungal homologues, and more similar to CE1s of bacteria, suggesting a horizontal gene transfer (HGT) event.
@article{GRL3_Mares_Chaib2014, title = {Horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal Amanita}, journal = {New Phytologist Foundation}, author = {Mares, Maryam Chaib De and Hess, Jaqueline and Floudas, Dimitrios and Lipzen, Anna and Choi, Cindy and Kennedy, Megan and Grigoriev, Igor V. and Pringle, Anne}, year = {2014}, doi = {10.1111/nph.13140}, link = {https://nph.onlinelibrary.wiley.com/doi/10.1111/nph.13140}, image_filename = {./images/publications/GRL3_Mares_Chaib2014.webp}, published = {1}, tag = {10004} }
“Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita”.
J. Hess, I. Skrede, M. C. D. Mares, M. Hainaut, B. Henrissat, and A. Pringle.
Oxford Academic, 2018
ABS BIB

Fungi are evolutionary shape shifters and adapt quickly to new environments. Ectomycorrhizal (EM) symbioses are mutualistic associations between fungi and plants and have evolved repeatedly and independently across the fungal tree of life, suggesting lineages frequently reconfigure genome content to take advantage of open ecological niches. To date analyses of genomic mechanisms facilitating EM symbioses have involved comparisons of distantly related species, but here, we use the genomes of three EM and two asymbiotic (AS) fungi from the genus Amanita as well as an AS outgroup to study genome evolution following a single origin of symbiosis. Our aim was to identify the defining features of EM genomes, but our analyses suggest no clear differentiation of genome size, gene repertoire size, or transposable element content between EM and AS species. Phylogenetic inference of gene gains and losses suggests the transition to symbiosis was dominated by the loss of plant cell wall decomposition genes, a confirmation of previous findings. However, the same dynamic defines the AS species A. inopinata, suggesting loss is not strictly associated with origin of symbiosis. Gene expansions in the common ancestor of EM Amanita were modest, but lineage specific and large gene family expansions are found in two of the three EM extant species. Even closely related EM genomes appear to share few common features. The genetic toolkit required for symbiosis appears already encoded in the genomes of saprotrophic species, and this dynamic may explain the pervasive, recurrent evolution of ectomycorrhizal associations
@article{GRL6_Mares_Chaib2018, title = {Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita}, journal = {Oxford Academic}, author = {Hess, Jaqueline and Skrede, Inger and Mares, Maryam Chaib De and Hainaut, Matthieu and Henrissat, Bernard and Pringle, Anne}, year = {2018}, doi = {10.1093/molbev/msy179}, link = {https://academic.oup.com/mbe/article/35/11/2786/5100885}, image_filename = {}, published = {1}, tag = {10004} }
“Functional and Phylogenetic Characterization of Bacteria in Bovine Rumen Using Fractionation of Ruminal Fluid”.
R. Hernández, M. C. D. Mares, H. Jimenez, A. Reyes, and A. Caro-Quintero.
frontiers, 2022
ABS BIB

Cattle productivity depends on our ability to fully understand and manipulate the fermentation process of plant material that occurs in the bovine rumen, which ultimately leads to the improvement of animal health and increased productivity with a reduction in environmental impact. An essential step in this direction is the phylogenetic and functional characterization of the microbial species composing the ruminal microbiota. To address this challenge, we separated a ruminal fluid sample by size and density using a sucrose density gradient. We used the full sample and the smallest fraction (5%), allowing the enrichment of bacteria, to assemble metagenome-assembled genomes (MAGs). We obtained a total of 16 bacterial genomes, 15 of these enriched in the smallest fraction of the gradient. According to the recently proposed Genome Taxonomy Database (GTDB) taxonomy, these MAGs belong to Bacteroidota, Firmicutes_A, Firmicutes, Proteobacteria, and Spirochaetota phyla
@article{GRL7_Mares_Chaib2022, title = {Functional and Phylogenetic Characterization of Bacteria in Bovine Rumen Using Fractionation of Ruminal Fluid}, journal = {frontiers}, author = {Hernández, Ruth and Mares, Maryam Chaib De and Jimenez, Hugo and Reyes, Alejandro and Caro-Quintero, Alejandro}, year = {2022}, doi = {10.3389/fmicb.2022.813002}, link = {https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2022.813002/full}, image_filename = {}, published = {1}, tag = {10004} }