Key Knowledge Gaps to Fill at the Cell-To-Ecosystem Level in Marine B-Vitamin Cycling

Abstract

B-vitamins are essential micronutrients for marine plankton. Additionally, we now know many marine plankton cannot synthesize B-vitamins de novo (from scratch) and thus are reliant on external supplies. Details of B-vitamin exchange, whether ‘active’ or ‘passive’ (i.e. through cell secretion or mortality), are lacking and as a result we struggle to predict microbial physiology, community composition and biogeochemistry. We argue that significant advances in understanding of the impact of B-vitamin exchange and cycling on marine community structure and biogeochemistry can be made by focusing on unknowns related to the ‘in’s and out’s’ of B-vitamin transport, exchange between plankton, and ecosystem scale processing/transformation of B-vitamins. We point out that it is particularly necessary to reach beyond traditional categorization of populations as B-vitamin auxotrophs (requiring supplied vitamin) or prototrophs (de novo vitamin synthesizers) and begin addressing which populations are net ‘providers’ and/or ‘consumers’. This is a particularly interesting problem as organisms cannot be confidently categorized as net ‘providers’ and/or ‘consumers’ based on genome-based prediction, and it is possible the two roles may change over time and environmental conditions. We posit that greater knowledge of B-vitamin exchange, e.g. cross-feeding, acquisition and secretion systems, environmental triggers of ‘provision’ and ‘consumption’, will reveal unforeseen networking and novel niches across marine planktonic communities. Last, we advocate for further experiments tracking the responses of isolates or natural communities relative to vitamin availability, tracing flow of B-vitamins between cells using novel approaches (e.g. isotopic, fluorometric), and greater consideration of altered B-vitamin exchange and cycling under future climate scenarios.

Seasonal and daily patterns in known dissolved metabolites in the northwestern Sargasso Sea

“…Two vitamins (pantothenic acid and riboflavin) and one vitamin precursor (desthiobiotin) showed higher concentrations in the mixed layer during the winter mixed period. The production and consumption of vitamins occurs in both phytoplankton and heterotrophic bacteria (Koch et al 2012; Rodionov et al 2003; Sañudo-Wilhelmy et al 2014; Warren et al 2002), and vitamins are exchanged within microbial communities (Joglar et al 2021; Wienhausen et al 2022a; Zoccarato et al 2022). Vitamin precursors may enable cellular growth in the absence of the vitamin itself, as has been observed in some, but not all, bacterial cells tested for the ability to use desthiobiotin in the absence of biotin (Wienhausen et al 2022b).…”

The overlooked role of a biotin precursor for marine bacteria - desthiobiotin as an escape route for biotin auxotrophy

“…The discrepancy between intracellular and extracellular biotin concentrations might be related to the fact that biotin is covalently bound to enzymes, therefore the cofactor might be intracellularly bound to enzymes and thus not fully captured by our extraction method. The mechanism by which B-vitamins, including biotin, are released is still largely unknown [59]. The chemical structure of desthiobiotin and biotin differs significantly, with biotin having a sulfur-containing tetrahydrothiophene ring fused to a ureido group.…”

Seasonal and daily patterns in known dissolved metabolites in the northwestern Sargasso Sea

“…Two vitamins (pantothenic acid and riboflavin) and one vitamin precursor (desthiobiotin) showed higher concentrations in the mixed layer during the winter mixed period. The production and consumption of vitamins occurs in both phytoplankton and heterotrophic bacteria (Warren et al 2002; Rodionov et al 2003; Koch et al 2012; Sañudo‐Wilhelmy et al 2014), and vitamins are exchanged within microbial communities (Joglar et al 2021; Wienhausen et al 2022 a ; Zoccarato et al 2022). Vitamin precursors may enable cellular growth in the absence of the vitamin itself, as has been observed in some, but not all, bacterial cells tested for the ability to use desthiobiotin in the absence of biotin (Wienhausen et al 2022 b ).…”