Metagenomic Evidence for Cobamide Producers Driving Prokaryotic Co-occurrence Associations and Potential Function in Wastewater Treatment Plants

Abstract

Cobamides are required by most organisms but are only produced by specific prokaryotic taxa. These commonly shared cofactors play significant roles in shaping the microbial community and ecosystem function. Wastewater treatment plants (WWTPs) are the world’s most common biotechnological systems; knowledge about sharing of cobamides among microorganisms is predicted to be important to decipher the complex microbial relationships in these systems. Herein, we explored prokaryotic potential cobamide producers in global WWTP systems based on metagenomic analyses. A set of 8253 metagenome-assembled genomes (MAGs) were recovered and 1276 (15.5%) of them were identified as cobamide producers, which could potentially be used for the practical biological manipulation of WWTP systems. Moreover, 8090 of the total recovered MAGs (98.0%) contained at least one enzyme family dependent on cobamides, indicating the sharing of cobamides among microbial members in WWTP systems. Importantly, our results showed that the relative abundance and number of cobamide producers improved the complexity of microbial co-occurrence networks and most nitrogen, sulfur, and phosphorus cycling gene abundances, indicating the significance of cobamides in microbial ecology and their potential function in WWTP systems. These findings enhance the knowledge of cobamide producers and their functions in WWTP systems, which has important implications for improving the efficiency of microbial wastewater treatment processes.

Skin-associated Corynebacterium amycolatum shares cobamides

“…Yet, mass spectrometry revealed very low levels of cobalamin (a benzimidazolyl cobamide) in the same cell extracts, supporting this prediction. A wealth of studies exist that predict the existence of cobamide sharing between microorganisms (9,(11)(12)(13)(14)(15)(16)(17)42), and of these, a number provide direct experimental evidence for this phenomenon, although they are almost exclusively restricted to those between bacteria and cobamide-requiring eukaryotes (43)(44)(45)(46). Evidence of cobamide sharing between two or more bacterial species is limited, potentially due to a lack of experimental models to measure this phenomenon and the non-auxotrophic nature of many cobamide-utilizing bacteria (9).…”

“…Cobamide sharing has been investigated in diverse ecosystems, including the human gut (6, 10, 11), marine environments (12–14), soil (15), wastewater treatment plants (16), and as we have shown recently, human skin (17). In the gut, approximately half of the known species rely on cobamides for metabolism, and numerous cobamide acquisition mechanisms exist for both cobamide producers and non-producers (18).…”

“…This disproportionate distribution of producers to users, combined with the centrality of cobamides to cellular function and selectivity of microbes towards particular cobamides, suggests that cobamide sharing occurs in microbial communities, and further, that cobamides drive community dynamics (8). Cobamide sharing has been investigated in diverse ecosystems, including the human gut (6,10,11), marine environments (12)(13)(14), soil (15), wastewater treatment plants (16), and as we have shown recently, human skin (17). In the gut, approximately half of the known species rely on cobamides for metabolism, and numerous cobamide acquisition mechanisms exist for both cobamide producers and non-producers (18).…”

Global biogeography and ecological implications of cobamide-producing prokaryotes

“…Processes for identifying potential producers of cobamide have been described in our previous study [ 36 ]. Briefly, Hidden Markov Model (HMM) profiles ( Supplementary Fig.…”

Biological Interactions Mediate Soil Functions by Altering Rare Microbial Communities

“…The adjusted P values were calculated by utilizing the Benjamini and Hochberg Procedure to control the false discovery rate. Network properties were calculated by “ggClusterNet” package to show the complexity of a co-occurrence network, including the number of edges, average degree, clustering coefficient, and centralization betweenness and connectance. , A structural equation model (SEM) was developed to evaluate the direct and indirect effects of different interactions among soil fauna, specific microbial abundance, and community on soil functional gene abundance using AMOS 21 (SPSS Inc., Chicago). For the microbial community, we employed the value of principal coordinate axis 1 from the PCoA plot to represent.…”