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1. Enrichable consortia of microbial symbionts degrade macroalgal polysaccharides in Kyphosus fish

   https://doi.org/10.1128/mbio.00496-24  

   Oliver, Aaron; Podell, Sheila; Wegley_Kelly, Linda; Sparagon, Wesley J; Plominsky, Alvaro M; Nelson, Robert S; Laurens, Lieve_M L; Augyte, Simona; Sims, Neil A; Nelson, Craig E; et al (May 2024, mBio)

   Martiny, Jennifer_B H (Ed.)

   Coastal herbivorous fishes consume macroalgae, which is then degraded by microbes along their digestive tract. However, there is scarce genomic information about the microbiota that perform this degradation. This study explores the potential ofKyphosusgastrointestinal microbial symbionts to collaboratively degrade and ferment polysaccharides from red, green, and brown macroalgae throughin silicostudy of carbohydrate-active enzyme and sulfatase sequences. Recovery of metagenome-assembled genomes (MAGs) from previously describedKyphosusgut metagenomes and newly sequenced bioreactor enrichments reveals differences in enzymatic capabilities between the major microbial taxa inKyphosusguts. The most versatile of the recovered MAGs were from theBacteroidotaphylum, whose MAGs house enzyme collections able to decompose a variety of algal polysaccharides. Unique enzymes and predicted degradative capacities of genomes from theBacillota(genusVallitalea) andVerrucomicrobiota(orderKiritimatiellales) highlight the importance of metabolic contributions from multiple phyla to broaden polysaccharide degradation capabilities. Few genomes contain the required enzymes to fully degrade any complex sulfated algal polysaccharide alone. The distribution of suitable enzymes between MAGs originating from different taxa, along with the widespread detection of signal peptides in candidate enzymes, is consistent with cooperative extracellular degradation of these carbohydrates. This study leverages genomic evidence to reveal an untapped diversity at the enzyme and strain level amongKyphosussymbionts and their contributions to macroalgae decomposition. Bioreactor enrichments provide a genomic foundation for degradative and fermentative processes central to translating the knowledge gained from this system to the aquaculture and bioenergy sectors.IMPORTANCESeaweed has long been considered a promising source of sustainable biomass for bioenergy and aquaculture feed, but scalable industrial methods for decomposing terrestrial compounds can struggle to break down seaweed polysaccharides efficiently due to their unique sulfated structures. Fish of the genusKyphosusfeed on seaweed by leveraging gastrointestinal bacteria to degrade algal polysaccharides into simple sugars. This study reconstructs metagenome-assembled genomes for these gastrointestinal bacteria to enhance our understanding of herbivorous fish digestion and fermentation of algal sugars. Investigations at the gene level identifyKyphosusguts as an untapped source of seaweed-degrading enzymes ripe for further characterization. These discoveries set the stage for future work incorporating marine enzymes and microbial communities in the industrial degradation of algal polysaccharides. 

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2. Herbivorous Fish Microbiome Adaptations to Sulfated Dietary Polysaccharides

   https://doi.org/10.1128/aem.02154-22  

   Podell, Sheila; Oliver, Aaron; Kelly, Linda Wegley; Sparagon, Wesley J.; Plominsky, Alvaro M.; Nelson, Robert S.; Laurens, Lieve M.; Augyte, Simona; Sims, Neil A.; Nelson, Craig E.; et al (May 2023, Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Marine herbivorous fish that feed primarily on macroalgae, such as those from the genus Kyphosus, are essential for maintaining coral health and abundance on tropical reefs. Here, deep metagenomic sequencing and assembly of gut compartment-specific samples from three sympatric, macroalgivorous Hawaiian kyphosid species have been used to connect host gut microbial taxa with predicted protein functional capacities likely to contribute to efficient macroalgal digestion. Bacterial community compositions, algal dietary sources, and predicted enzyme functionalities were analyzed in parallel for 16 metagenomes spanning the mid- and hindgut digestive regions of wild-caught fishes. Gene colocalization patterns of expanded carbohydrate (CAZy) and sulfatase (SulfAtlas) digestive enzyme families on assembled contigs were used to identify likely polysaccharide utilization locus associations and to visualize potential cooperative networks of extracellularly exported proteins targeting complex sulfated polysaccharides. These insights into the gut microbiota of herbivorous marine fish and their functional capabilities improve our understanding of the enzymes and microorganisms involved in digesting complex macroalgal sulfated polysaccharides. IMPORTANCE This work connects specific uncultured bacterial taxa with distinct polysaccharide digestion capabilities lacking in their marine vertebrate hosts, providing fresh insights into poorly understood processes for deconstructing complex sulfated polysaccharides and potential evolutionary mechanisms for microbial acquisition of expanded macroalgal utilization gene functions. Several thousand new marine-specific candidate enzyme sequences for polysaccharide utilization have been identified. These data provide foundational resources for future investigations into suppression of coral reef macroalgal overgrowth, fish host physiology, the use of macroalgal feedstocks in terrestrial and aquaculture animal feeds, and the bioconversion of macroalgae biomass into value-added commercial fuel and chemical products. 

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3. Relative Importance of Macroalgae and Phytoplankton to Nearshore Consumers and Growth Across Climatic Conditions in the Northern Gulf of Alaska

   https://doi.org/10.1007/s12237-024-01371-6  

   Corliss, Katherine; von_Biela, Vanessa; Coletti, Heather; Bodkin, James; Esler, Daniel; Iken, Katrin (September 2024, Estuaries and Coasts)

   Abstract Macroalgae and phytoplankton support the base of highly productive nearshore ecosystems in cold-temperate regions. To better understand their relative importance to nearshore food webs, this study considered four regions in the northern Gulf of Alaska where three indicator consumers were collected, filter-feeding mussels (Mytilus trossulus), pelagic-feeding Black Rockfish (Sebastes melanops), and benthic-feeding Kelp Greenling (Hexagrammos decagrammus). The study objectives were to (1) estimate the proportional contributions of macroalgal and phytoplankton organic matter using carbon and nitrogen stable isotopes, (2) determine if macroalgal use affected consumer growth using annual growth rings in shells or otoliths, and (3) describe changes in organic matter use and growth during the Pacific Marine Heatwave (PMH; 2014–2016) in one consumer, mussels. Macroalgae were the major organic matter source (> 60%) to the diet for all three consumers. The relationships between macroalgal contribution and growth were neutral for both fish species and significantly positive for mussels. During the PMH, mussels had a drop (> 10%) in macroalgal contributions and grew 45% less than in other time periods. Simultaneously, the relationship between macroalgal contribution and mussel growth was strongest during the PMH, explaining 48% variation compared to 3–12% before or after the PMH. Collectively, the results suggest that macroalgae is likely more important to cold-temperate nearshore food webs than phytoplankton. Management actions aimed at conserving and expanding macroalgae are likely to benefit nearshore food webs under all climate scenarios and especially during marine heatwaves. 

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4. Brockarchaeota, a novel archaeal phylum with unique and versatile carbon cycling pathways

   https://doi.org/10.1038/s41467-021-22736-6  

   De Anda, Valerie; Chen, Lin-Xing; Dombrowski, Nina; Hua, Zheng-Shuang; Jiang, Hong-Chen; Banfield, Jillian F.; Li, Wen-Jun; Baker, Brett J. (December 2021, Nature Communications)

   Abstract Geothermal environments, such as hot springs and hydrothermal vents, are hotspots for carbon cycling and contain many poorly described microbial taxa. Here, we reconstructed 15 archaeal metagenome-assembled genomes (MAGs) from terrestrial hot spring sediments in China and deep-sea hydrothermal vent sediments in Guaymas Basin, Gulf of California. Phylogenetic analyses of these MAGs indicate that they form a distinct group within the TACK superphylum, and thus we propose their classification as a new phylum, ‘Brockarchaeota’, named after Thomas Brock for his seminal research in hot springs. Based on the MAG sequence information, we infer that some Brockarchaeota are uniquely capable of mediating non-methanogenic anaerobic methylotrophy, via the tetrahydrofolate methyl branch of the Wood-Ljungdahl pathway and reductive glycine pathway. The hydrothermal vent genotypes appear to be obligate fermenters of plant-derived polysaccharides that rely mostly on substrate-level phosphorylation, as they seem to lack most respiratory complexes. In contrast, hot spring lineages have alternate pathways to increase their ATP yield, including anaerobic methylotrophy of methanol and trimethylamine, and potentially use geothermally derived mercury, arsenic, or hydrogen. Their broad distribution and their apparent anaerobic metabolic versatility indicate that Brockarchaeota may occupy previously overlooked roles in anaerobic carbon cycling. 

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5. The Biogeochemistry of Marine Polysaccharides: Sources, Inventories, and Bacterial Drivers of the Carbohydrate Cycle

   https://doi.org/10.1146/annurev-marine-032020-012810  

   Arnosti, C.; Wietz, M.; Brinkhoff, T.; Hehemann, J.-H.; Probandt, D.; Zeugner, L.; Amann, R. (January 2021, Annual Review of Marine Science)

   null (Ed.)

   Polysaccharides are major components of macroalgal and phytoplankton biomass and constitute a large fraction of the organic matter produced and degraded in the ocean. Until recently, however, our knowledge of marine polysaccharides was limited due to their great structural complexity, the correspondingly complicated enzymatic machinery used by microbial communities to degrade them, and a lack of readily applied means to isolate andcharacterize polysaccharides in detail. Advances in carbohydrate chemistry, bioinformatics, molecular ecology, and microbiology have led to new insights into the structures of polysaccharides, the means by which they are degraded by bacteria, and the ecology of polysaccharide production and decomposition. Here, we survey current knowledge, discuss recent advances, and present a new conceptual model linking polysaccharide structural complexity and abundance to microbially driven mechanisms of polysaccharide processing. We conclude by highlighting specific future research foci that will shed light on this central but poorly characterized component of the marine carbon cycle. 

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