Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy

Ferrer‐González, Frank X.; Widner, Brittany; Holderman, Nicole R.; Glushka, John; Edison, Arthur S.; Kujawinski, Elizabeth B.; Moran, Mary Ann

doi:10.1038/s41396-020-00811-y

Cited by 103 publications

(118 citation statements)

References 104 publications

Supporting

Mentioning

111

Contrasting

Order By: Relevance

“…N-based growth rates of Asterionella -associated bacteria were up to twice as fast as for their free-living counterparts, although nitrate was replete in the medium for both free-living and cell-associated bacteria. We therefore presume that the growth of diatom-associated bacteria within the phycosphere was promoted by the provision of, for example, sulfur, trace metals, and detoxifying byproducts, besides C and N, as common in diatom–bacteria interactions ( 72 , 74 – 78 ).…”

Section: Discussionmentioning

confidence: 99%

Characterizing the “fungal shunt”: Parasitic fungi on diatoms affect carbon flow and bacterial communities in aquatic microbial food webs

Klawonn

Wyngaert

Parada

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Microbial interactions in aquatic environments profoundly affect global biogeochemical cycles, but the role of microparasites has been largely overlooked. Using a model pathosystem, we studied hitherto cryptic interactions between microparasitic fungi (chytrid Rhizophydiales), their diatom host Asterionella, and cell-associated and free-living bacteria. We analyzed the effect of fungal infections on microbial abundances, bacterial taxonomy, cell-to-cell carbon transfer, and cell-specific nitrate-based growth using microscopy (e.g., fluorescence in situ hybridization), 16S rRNA gene amplicon sequencing, and secondary ion mass spectrometry. Bacterial abundances were 2 to 4 times higher on individual fungal-infected diatoms compared to healthy diatoms, particularly involving Burkholderiales. Furthermore, taxonomic compositions of both diatom-associated and free-living bacteria were significantly different between noninfected and fungal-infected cocultures. The fungal microparasite, including diatom-associated sporangia and free-swimming zoospores, derived ∼100% of their carbon content from the diatom. By comparison, transfer efficiencies of photosynthetic carbon were lower to diatom-associated bacteria (67 to 98%), with a high cell-to-cell variability, and even lower to free-living bacteria (32%). Likewise, nitrate-based growth for the diatom and fungi was synchronized and faster than for diatom-associated and free-living bacteria. In a natural lacustrine system, where infection prevalence reached 54%, we calculated that 20% of the total diatom-derived photosynthetic carbon was shunted to the parasitic fungi, which can be grazed by zooplankton, thereby accelerating carbon transfer to higher trophic levels and bypassing the microbial loop. The herein termed “fungal shunt” can thus significantly modify the fate of photosynthetic carbon and the nature of phytoplankton–bacteria interactions, with implications for diverse pelagic food webs and global biogeochemical cycles.

show abstract

Section: Discussionmentioning

confidence: 99%

Characterizing the “fungal shunt”: Parasitic fungi on diatoms affect carbon flow and bacterial communities in aquatic microbial food webs

Klawonn

Wyngaert

Parada

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…Polysaccharides constitute a major fraction of the algae-derived organic matter, with important roles in nutrient cycles and microbial metabolism (Hehemann et al, 2014;Arnosti et al, 2021). Consequently, diverse bacteria are specialized for the degradation of algal polysaccharides, colonization of algal surfaces and other types of biological interactions (van der Loos et al, 2019;Ferrer-González et al, 2020;Wolter et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

CAZymes in Maribacter dokdonensis 62–1 From the Patagonian Shelf: Genomics and Physiology Compared to Related Flavobacteria and a Co-occurring Alteromonas Strain

et al. 2021

View full text Add to dashboard Cite

Carbohydrate-active enzymes (CAZymes) are an important feature of bacteria in productive marine systems such as continental shelves, where phytoplankton and macroalgae produce diverse polysaccharides. We herein describe Maribacter dokdonensis 62–1, a novel strain of this flavobacterial species, isolated from alginate-supplemented seawater collected at the Patagonian continental shelf. M. dokdonensis 62–1 harbors a diverse array of CAZymes in multiple polysaccharide utilization loci (PUL). Two PUL encoding polysaccharide lyases from families 6, 7, 12, and 17 allow substantial growth with alginate as sole carbon source, with simultaneous utilization of mannuronate and guluronate as demonstrated by HPLC. Furthermore, strain 62-1 harbors a mixed-feature PUL encoding both ulvan- and fucoidan-targeting CAZymes. Core-genome phylogeny and pangenome analysis revealed variable occurrence of these PUL in related Maribacter and Zobellia strains, indicating specialization to certain “polysaccharide niches.” Furthermore, lineage- and strain-specific genomic signatures for exopolysaccharide synthesis possibly mediate distinct strategies for surface attachment and host interaction. The wide detection of CAZyme homologs in algae-derived metagenomes suggests global occurrence in algal holobionts, supported by sharing multiple adaptive features with the hydrolytic model flavobacterium Zobellia galactanivorans. Comparison with Alteromonas sp. 76-1 isolated from the same seawater sample revealed that these co-occurring strains target similar polysaccharides but with different genomic repertoires, coincident with differing growth behavior on alginate that might mediate ecological specialization. Altogether, our study contributes to the perception of Maribacter as versatile flavobacterial polysaccharide degrader, with implications for biogeochemical cycles, niche specialization and bacteria-algae interactions in the oceans.

show abstract

“…Consequently, diverse bacteria are specialized for the degradation of algal polysaccharides, colonization of algal surfaces and other types of biological interactions (van der Loos et al 2019, Wolter et al 2020, Ferrer-González et al 2020.…”

Section: Introductionmentioning

confidence: 99%

CAZymes inMaribacter dokdonensis62-1 from the Patagonian shelf: Genomics and physiology compared to related flavobacteria and a co-occurringAlteromonasstrain

Wolter

Mitulla

Kalem

et al. 2020

Preprint

View full text Add to dashboard Cite

Carbohydrate-active enzymes (CAZymes) are an important feature of bacteria in productive marine systems such as continental shelves, where phytoplankton and macroalgae produce diverse polysaccharides. We herein describe Maribacter dokdonensis 62-1, a novel strain of this flavobacterial species, isolated from alginate-supplemented seawater collected at the Patagonian continental shelf. M. dokdonensis 62-1 harbors a diverse array of CAZymes in multiple polysaccharide utilization loci (PUL). Two PUL encoding polysaccharide lyases from families 6, 7, 12 and 17 allow substantial growth with alginate as sole carbon source, with simultaneous utilization of mannuronate and guluronate as demonstrated by HPLC. Furthermore, strain 62-1 harbors a mixed-feature PUL encoding both ulvan- and fucoidan-targeting CAZymes. Core-genome phylogeny and pangenome analysis revealed variable occurrence of these PUL in related Maribacter and Zobellia strains, indicating specialization to certain “polysaccharide niches”. Furthermore, lineage- and strain-specific genomic signatures for exopolysaccharide synthesis possibly mediate distinct strategies for surface attachment and host interaction. The wide detection of CAZyme homologs in algae-derived metagenomes suggests global occurrence in algal holobionts, supported by sharing multiple adaptive features with the hydrolytic model flavobacterium Zobellia galactanivorans. Comparison with Alteromonas sp. 76-1 isolated from the same seawater sample revealed that these co-occurring strains target similar polysaccharides but with different genomic repertoires, coincident with differing growth behavior on alginate that might mediate ecological specialization. Altogether, our study contributes to the perception of Maribacter as versatile flavobacterial polysaccharide degrader, with implications for biogeochemical cycles, niche specialization and bacteria-algae interactions in the oceans.

show abstract

Resource partitioning of phytoplankton metabolites that support bacterial heterotrophy

Cited by 103 publications

References 104 publications

Characterizing the “fungal shunt”: Parasitic fungi on diatoms affect carbon flow and bacterial communities in aquatic microbial food webs

Characterizing the “fungal shunt”: Parasitic fungi on diatoms affect carbon flow and bacterial communities in aquatic microbial food webs

CAZymes in Maribacter dokdonensis 62–1 From the Patagonian Shelf: Genomics and Physiology Compared to Related Flavobacteria and a Co-occurring Alteromonas Strain

CAZymes inMaribacter dokdonensis62-1 from the Patagonian shelf: Genomics and physiology compared to related flavobacteria and a co-occurringAlteromonasstrain

Contact Info

Product

Resources

About