Transcriptomic Study of Substrate-Specific Transport Mechanisms for Iron and Carbon in the Marine Copiotroph Alteromonas macleodii

Abstract

Iron is an essential micronutrient for all microbial growth in the marine environment, and in heterotrophic bacteria, iron is tightly linked to carbon metabolism due to its central role as a cofactor in enzymes of the respiratory chain. Here, we present the iron- and carbon-regulated transcriptomes of a representative marine copiotroph, Alteromonas macleodii ATCC 27126, and characterize its cellular transport mechanisms. ATCC 27126 has distinct metabolic responses to iron and carbon limitation and, accordingly, uses distinct sets of TonB-dependent transporters for the acquisition of iron and carbon. These distinct sets of TonB-dependent transporters were of a similar number, indicating that the diversity of carbon and iron substrates available to ATCC 27126 is of a similar scale. For the first time in a marine bacterium, we have also identified six characteristic inner membrane permeases for the transport of siderophores via an ATPase-independent mechanism. An examination of the distribution of specific TonB-dependent transporters in 31 genomes across the genus Alteromonas points to niche specialization in transport capacity, particularly for iron. We conclude that the substrate-specific bioavailability of both iron and carbon in the marine environment will likely be a key control on the processing of organic matter through the microbial loop. IMPORTANCE As the major facilitators of the turnover of organic matter in the marine environment, the ability of heterotrophic bacteria to acquire specific compounds within the diverse range of dissolved organic matter will affect the regeneration of essential nutrients such as iron and carbon. TonB-dependent transporters are a prevalent cellular tool in Gram-negative bacteria that allow a relatively high-molecular-weight fraction of organic matter to be directly accessed. However, these transporters are not well characterized in marine bacteria, limiting our understanding of the flow of specific substrates through the marine microbial loop. Here, we characterize the TonB-dependent transporters responsible for iron and carbon acquisition in a representative marine copiotroph and examine their distribution across the genus Alteromonas. We provide evidence that substrate-specific bioavailability is niche specific, particularly for iron complexes, indicating that transport capacity may serve as a significant control on microbial community dynamics and the resultant cycling of organic matter.

Genome and Ecology of a NovelAlteromonasPodovirus, ZP6, Representing a New Viral Genus,Mareflavirus

“…Alteromonas has been found to make significant contributions to iron metabolism ( 20 , 21 ) and play an important role in marine organic carbon and nitrogen cycling ( 22 ). In laboratory cocultures with cyanobacteria like Prochlorococcus , Synechococcus , and Trichodesmium ( 23 ), Alteromonas has demonstrated broad substrate preferences and can utilize dissolved organic carbon and particulate organic carbon supplied by photoautotrophs ( 24 ).…”

Post-translational flavinylation is associated with diverse extracytosolic redox functionalities throughout bacterial life

“…Finally, PepSY-like gene clusters have been shown to be repressed by Fur (the primary transcription regulator that responds to iron limitation) in Shewanella oneidensis and Caulobacter crescentus ( da Silva Neto et al, 2013 ; Wan et al, 2004 ). Moreover, in some cases, PepSY-like proteins may be actively involved in the extraction of siderophore-bound iron, as periplasmic reduction has been shown to be important for the uptake of siderophore-bound iron and 231 PepSY-like gene clusters encode a TonB receptor (Pfam accession PF03544) related to well-characterized outer membrane siderophore transporters ( Figure 4C ; Liu et al, 2018a ; Manck et al, 2020 ).…”

Prochlorococcus exudate stimulates heterotrophic bacterial competition with rival phytoplankton for available nitrogen

“…Consequently, C-starved cells have diminished rates of ammonium assimilation and potentially other N utilization pathways, even when cells are N limited (77). Notably, a recent study found that Alteromonas significantly reduced expression of genes involved in nitrogen metabolic pathways under carbon and iron colimitation (78).…”