Evidence of Interdomain Ammonium Cross-Feeding From Methylamine- and Glycine Betaine-Degrading Rhodobacteraceae to Diatoms as a Widespread Interaction in the Marine Phycosphere

Abstract

Dissolved organic nitrogen (DON) compounds such as methylamines (MAs) and glycine betaine (GBT) occur at detectable concentrations in marine habitats and are also produced and released by microalgae. For many marine bacteria, these DON compounds can serve as carbon, energy, and nitrogen sources, but microalgae usually cannot metabolize them. Interestingly though, it was previously shown that Donghicola sp. strain KarMa—a member of the marine Rhodobacteraceae —can cross-feed ammonium such that the ammonium it produces upon degrading monomethylamine (MMA) then serves as nitrogen source for the diatom Phaeodactylum tricornutum ; thus, these organisms form a mutual metabolic interaction under photoautotrophic conditions. In the present study, we investigated whether this interaction plays a broader role in bacteria–diatom interactions in general. Results showed that cross-feeding between strain KarMa and P. tricornutum was also possible with di- and trimethylamine as well as with GBT. Further, cross-feeding of strain KarMa was also observed in cocultures with the diatoms Amphora coffeaeformis and Thalassiosira pseudonana with MMA as the sole nitrogen source. Regarding cross-feeding involving other Rhodobacteraceae strains, the in silico analysis of MA and GBT degradation pathways indicated that algae-associated Rhodobacteraceae -type strains likely interact with P. tricornutum in a similar manner as the strain KarMa does. For these types of strains (such as Celeribacter halophilus , Roseobacter denitrificans , Roseovarius indicus , Ruegeria pomeroyi , and Sulfitobacter noctilucicola ), ammonium cross-feeding after methylamine degradation showed species-specific patterns, whereas bacterial GBT degradation always led to diatom growth. Overall, the degradation of DON compounds by the Rhodobacteraceae family and the subsequent cross-feeding of ammonium may represent a widespread, organism-specific, and regulated metabolic interaction for establishing and stabilizing associations with photoautotrophic diatoms in the oceans.

Microbial uptake dynamics of choline and glycine betaine in coastal seawater

“…It can further be expected that the phytoplankton and microzooplankton intracellular choline/GBT pool is not immediately available for microbial uptake, because of a delayed release from cells to the DOM pool depending on, for example, cell degradation, sloppy feeding, or viral lysis. Thus, an alternative explanation for the observed correlation pattern might lie in a recent study suggesting that cross‐feeding of ammonium between Rhodobacteraceae bacteria and their associated diatoms constitutes a widespread metabolic interaction (Zecher et al 2020) explaining their co‐occurrence. To support this hypothesis, further research would be required, though.…”

“…In summary, our data suggest that SST, salinity, and PON function as the main drivers of choline uptake which was largely driven by Rhodobacteraceae and, like their abundance, showed seasonal variation. Rhodobacteraceae are known for their interaction with phytoplankton, especially diatoms (Zecher et al 2020). Similarly, prokaryotic GBT uptake was influenced mainly by SST, salinity, and macronutrients (nitrogen, ).…”

Sensitivity of the mangrove-estuarine microbial community to aquaculture effluent

“…GBT degradation I was one of the major pathways contributing to the differences observed between low and high disturbed sites ( Figures 6 and S3 ). GBT is an important source of nitrogen in oligotrophic systems, acts as an organic osmolyte, and plays an important role in phytoplankton-bacteria interactions ( Becker et al., 2019 ; Jones et al, 2019 ; Zecher et al., 2020 ). The intertidal coastal mangrove ecosystem experiences daily fluctuations in a range of environmental conditions, including water levels and salinity.…”

Genome Analysis of Celeribacter sp. PS-C1 Isolated from Sekinchan Beach in Selangor, Malaysia, Reveals Its β-Glucosidase and Licheninase Activities

“…Earlier studies using whole cells suggested that Celeribacter spp. could potentially be used in bioremediation processes of heavy metals [10], organic compounds [11][12][13][14], volatile substances [15], and hydrocarbons [16][17][18]. Members of this genus are halophiles and Gram-negative, rod-shaped bacteria that thrive in various marine habitats (e.g., seawater, sea sediments, and mangrove soil) [19][20][21].…”

“…1.22), and α-L-arabinofuranosidase (EC 3.2.1.55). In the CAZy database, hemicelluloses were classified in the GH families 2,5,6,7,8,9,10,11,12,16,26,30,31,36,43,44,45,48,51,61,74,95, and 124 [37,39]. Ligninolytic enzymes (e.g., laccase, EC 1.10.3.2; lignin peroxidase, EC 1.11.1.7; and manganese peroxidase, EC 1.11.1.13) are involved in the breakdown of lignin and primarily belong to the CAZy auxiliary activities (AA) families AA1 to AA7 [37,40].…”