Forchielli, E. J. | Search bioRxiv

bioRxiv2024

Diversity in the Utilization of Different Molecular Classes of Dissolved Organic Matter by Heterotrophic Marine Bacteria

Heterotrophic marine bacteria utilize and recycle dissolved organic matter (DOM), impacting biogeochemical cycles. It is currently unclear to what extent distinct DOM components can be utilized by different heterotrophic clades. Here, we ask how a natural microbial community from the Eastern Mediterranean Sea responds to different molecular classes of DOM. These molecular classes - peptides, amino acids, amino sugars, disaccharides, monosaccharides and organic acids - together comprise much of the biomass of living organisms, released upon their death as DOM. Bulk bacterial activity increased after 24-hours for all treatments relative to the control, while glucose and ATP uptake decreased or remained unchanged. The relative abundance of several bacterial families, assessed using 16S rRNA amplicon sequencing, increased in some treatments: peptides promoted an increase in Pseudoalteromonadaceae, disaccharides promoted both Pseudoalteromonadaceae and Alteromonadaceae, and most other treatments were dominated by Vibrionaceae. While some results were consistent with recent laboratory-based studies, for example Pseudoalteromonadaceae favoring peptides, other clades behaved differently. Alteromonadaceae, for example, grew well in the lab on many substrates but dominated in seawater samples when disaccharides were added. These results highlight the diversity in DOM utilization among heterotrophic bacteria and complexities in the response of natural communities. ImportanceThe marine DOM pool contains numerous molecular classes, which change depending on the phytoplankton species, environmental conditions and interactions with other microbes, viruses and predators. In turn, the availability of these macromolecular pools affects the composition and function of the whole microbial community. Tracing the path between different carbon sources to specific microbes is another step towards revealing the dynamic interaction between bacteria and the DOM pool. This is especially important in warm and oligotrophic marine systems (e.g., Eastern Mediterranean Sea) where nutrients are scarce and may therefore affect microbial activity and growth.

microbiology↗

bioRxiv2022

Metabolic phenotyping of marine heterotrophs on refactored media reveals diverse metabolic adaptations and lifestyle strategies

Microbial communities, through their metabolism, drive carbon cycling in marine environments. These complex communities are composed of many different microorganisms including heterotrophic bacteria, each with its own nutritional needs and metabolic capabilities. Yet, models of ecosystem processes typically treat heterotrophic bacteria as a "black box", which does not resolve metabolic heterogeneity nor address ecologically important processes such as the successive modification of different types of organic matter. Here we directly address the heterogeneity of metabolism by characterizing the carbon source utilization preferences of 63 heterotrophic bacteria representative of several major marine clades. By systematically growing these bacteria on 10 media containing specific subsets of carbon sources found in marine biomass, we obtained a phenotypic fingerprint that we used to explore the relationship between metabolic preferences and phylogenetic or genomic features. At the class level, these bacteria display broadly conserved patterns of preference for different carbon sources. Despite these broad taxonomic trends, growth profiles correlate poorly with phylogenetic distance or genome-wide gene content. However, metabolic preferences are strongly predicted by a handful of key enzymes that preferentially belong to a few enriched metabolic pathways, such as those involved in glyoxylate metabolism and biofilm formation. We find that enriched pathways point to enzymes directly involved in the metabolism of the corresponding carbon source and suggest potential associations between metabolic preferences and other ecologically-relevant traits. The availability of systematic phenotypes across multiple synthetic media constitutes a valuable resource for future quantitative modeling efforts and systematic studies of inter-species interactions. ImportanceHalf of the Earths annual primary production is carried out by phytoplankton in the surface ocean. However, this metabolic activity is heavily impacted by heterotrophic bacteria, which dominate the transformation of organic matter released from phytoplankton. Here, we characterize the diversity of metabolic preferences across many representative heterotrophs by systematically growing them on different fractions of dissolved organic carbon (DOC). Our analysis suggests that different clades of bacteria have substantially distinct preferences for specific carbon sources, in a way that cannot be simply mapped onto phylogeny. These preferences are associated with the presence of specific genes and pathways, reflecting an association between metabolic capabilities and ecological lifestyles. In addition to helping understand the importance of heterotrophs under different conditions, the phenotypic fingerprint we obtained can help build higher resolution quantitative models of global microbial activity and biogeochemical cycles in the oceans.

microbiology↗