Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation

Abstract

BackgroundBiogeochemical elemental cycling is driven by primary production of biomass via phototrophic phytoplankton growth, with 40% of marine productivity being assigned to diatoms. Phytoplankton growth is widely limited by the availability of iron, an essential component of the photosynthetic apparatus. The oceanic diatom Thalassiosira oceanica shows a remarkable tolerance to low-iron conditions and was chosen as a model for deciphering the cellular response upon shortage of this essential micronutrient.ResultsThe combined efforts in genomics, transcriptomics and proteomics reveal an unexpected metabolic flexibility in response to iron availability for T. oceanica CCMP1005. The complex response comprises cellular retrenchment as well as remodeling of bioenergetic pathways, where the abundance of iron-rich photosynthetic proteins is lowered, whereas iron-rich mitochondrial proteins are preserved. As a consequence of iron deprivation, the photosynthetic machinery undergoes a remodeling to adjust the light energy utilization with the overall decrease in photosynthetic electron transfer complexes.ConclusionsBeneficial adaptations to low-iron environments include strategies to lower the cellular iron requirements and to enhance iron uptake. A novel contribution enhancing iron economy of phototrophic growth is observed with the iron-regulated substitution of three metal-containing fructose-bisphosphate aldolases involved in metabolic conversion of carbohydrates for enzymes that do not contain metals. Further, our data identify candidate components of a high-affinity iron-uptake system, with several of the involved genes and domains originating from duplication events. A high genomic plasticity, as seen from the fraction of genes acquired through horizontal gene transfer, provides the platform for these complex adaptations to a low-iron world.

Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom

“…To refine these results, we developed a stringent classification method which, starting from the clusters of orthologous proteins, generated > 9000 phylogenetic trees containing at least one P. multistriata protein and, based on the topology of each tree, predicted 252 genes of bacterial origin specifically within diatoms. This is < 50% of the number of genes reported to be of bacterial origin in P. tricornutum (587 genes) (Bowler et al ., 2008) and more than a previous estimate at lower resolution (Lommer et al ., 2012). Repeating the analysis considering HGT events within Stramenopiles and the SAR supergroup (Stramenopiles, Alveolates and Rhizaria), we predicted 353 and 438 P. multistriata genes of potential bacterial origin, respectively.…”

“…The genome size, N50 value and GC content were taken from the respective publications (Armbrust et al ., 2004; Bowler et al ., 2008; Cock et al ., 2010; Lévesque et al ., 2010; Lommer et al ., 2012; Tanaka et al ., 2015; Mock et al ., 2017). …”

“…These genomes contributed towards an understanding of the genes and pathways involved in nutrient assimilation and metabolism of diatoms. To improve our understanding of the evolution and adaptation of this highly diverse group of organisms, additional diatom genomes were sequenced, such as those of the open‐ocean centric diatom Thalassiosira oceanica (Lommer et al ., 2012), the oleaginous Fistulifera solaris (Tanaka et al ., 2015) and the polar diatom Fragilariopsis cylindrus (Mock et al ., 2017), instrumental for the study of iron physiology, lipid metabolism and adaptation to cold, respectively.…”

Transcriptional responses of three model diatoms to nitrate limitation of growth

“…First, a small percentage of proteins within each diatom belong to multi-copy gene families that commonly displayed different transcriptional patterns both within individual diatoms, as well as among the different diatoms. The extent of the genetic flexibility created by gene families may affect where and when nutrients are moved through the cell, ultimately influencing the flow of carbon and nitrogen (Lommer et al, 2012;Smith et al, 2012). For example, each diatom encodes multiple ammonium transporters, at least twice as many as the urea and nitrate transporters (Allen, 2005).…”

Central role for ferritin in the day/night regulation of iron homeostasis in marine phytoplankton

“…Earlier studies have shown that the uptake rates per unit of cell surface are similar among species with different iron requirements and as a consequence smaller cells with higher surface-to-volume ratios are favored under iron limitation (10,11). Acclimation to low iron induces rapid changes in the Photosystem (PS) II-to-PSI ratio and a global remodeling of the photosynthetic machinery (12), the down-regulation of nitrogen-reducing enzymes such as Fe-dependent nitrate and nitrite reductases, and the upregulation of enzymes involved in nitrogen recycling (13). In oceanic diatoms, metabolic adaptation to iron limitation involves a decrease of PSI and cytochrome b6/f requirements (14) and the utilization of copper-dependent plastocyanin instead of cytochrome c 6 (15,16).…”