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.
Highlights
In the oceans, diatoms (Bacillariophyceae) are ubiquitous microalgae that are important in the biogeochemical cycles of carbon and nitrogen (Smetacek, 1999)
To identify the potential carbon and nitrogen sources that the heterotrophic strain KarMa might receive from the photoautotrophic diatom P. tricornutum, in bacterial monocultures, we tested as growth substrates various carbohydrates, carboxylic acids, as well as amino acids and further Dissolved organic nitrogen (DON) compounds that may be actively or passively released by diatoms (Table 1)
Cocultivation of Strain KarMa and P. tricornutum With Various Nitrogen Sources. We investigated whether those organic nitrogen sources that could be utilized by strain KarMa and that are known to occur as DON in the marine water column can support the growth of P. tricornutum when offered as the sole nitrogen source in coculture with strain KarMa
Summary
Diatoms (Bacillariophyceae) are ubiquitous microalgae that are important in the biogeochemical cycles of carbon and nitrogen (Smetacek, 1999). A major reason why heterotrophic bacteria establish transient and permanent interactions with diatoms is that diatoms perform autotrophic CO2 fixation, which causes them to exude dissolved organic carbon (DOC) (Amin et al, 2012) made up of various carbohydrates (Passow, 2002; Grossart et al, 2006, 2007; Molino and Wetherbee, 2008; Agogué et al, 2014; Klein et al, 2014; Buhmann et al, 2016; Doghri et al, 2017) as well as free amino acids and proteins (Gärdes et al, 2012; Paul et al, 2013; Amin et al, 2015; Durham et al, 2015; Stahl and Ullrich, 2016). Bacteria provide diatoms and phytoplankton with growth promoters such as B vitamins and their precursors as well as indole-acetic acid (Bertrand et al, 2013; Amin et al, 2015; Wienhausen et al, 2017)
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