Recent Insights into the Diversity and Evolution of Invertebrate Hemerythrins and Extracellular Globins

Costa-Paiva, Elisa Maria; Coates, Christopher J.

doi:10.1007/978-3-030-41769-7_10

Cited by 3 publications

(4 citation statements)

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“…We therefore suggest an alternative hypothesis for the role and timing of the origins of oxygen-binding proteins in the animal lineage: that they may have evolved in response to rising oxygen levels in the environment, allowing larger multicellular organisms to then exploit the increased metabolic potential of abundant environmental oxygen. Our hypothesis is consistent with the fact that oxygen binding globins and hemerythrins appear to have an origin circa the common ancestor of bilateria [17,19,[29][30][31]. These proteins also first originate in the Ediacaran period, after the Neoproterozoic oxygenation event in which oxygen levels rose to near today's values [40,52].…”

Section: Discussionsupporting

confidence: 89%

“…These more primitive proteins were expressed in body cells and tissues, but still served to facilitate oxygen diffusion from cell to cell and through tissues by increasing the effective diffusion rate of oxygen much as modern tissue globins such as myoglobin do today [21][22][23][24][25][26][27][28]. The ancestral genes encoding these simple intracellular oxygen diffusion facilitators likely originated prior to most recent common ancestor of bilateria [17,19,[29][30][31], a critical clade in animal evolution which is defined by the origin of triploblastic embryos with endoderm, ectoderm and mesoderm germ layers which give rise to complex tissues more than two cells thick [32].…”

Section: Introductionmentioning

confidence: 99%

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Examining the role of oxygen-binding proteins on the early evolution of multicellularity

Wong,

Bravo,

Yunker

et al. 2023

Preprint

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Oxygen availability is a key factor in the evolution of multicellularity, as larger and more sophisticated organisms often require mechanisms allowing efficient oxygen delivery to their tissues. One such mechanism is the presence of oxygen-binding proteins, such as globins and hemerythrins, which arose in the ancestor of bilaterian animals. Despite their importance, the precise mechanisms by which oxygen-binding proteins influenced the early stages of multicellular evolution under varying environmental oxygen levels are not yet clear. We addressed this knowledge gap by heterologously expressing the oxygen binding proteins myoglobin and myohemerythrin in snowflake yeast, a model system of simple, undifferentiated multicellularity. These proteins increased the depth and rate of oxygen diffusion, increasing the fitness of snowflake yeast growing aerobically. Experiments show that, paradoxically, oxygen-binding proteins confer a greater fitness benefit for larger organisms under high, not low, O2conditions. We show via biophysical modeling that this is because facilitated diffusion is more efficient when oxygen is abundant, transporting a greater quantity of O2which can be used for metabolism. By alleviating anatomical diffusion limitations to oxygen consumption, the evolution of O2-binding proteins in the oxygen-rich Neoproterozoic may have been a key breakthrough enabling the evolution of increasingly large, complex multicellular metazoan lineages.

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Section: Discussionsupporting

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Examining the role of oxygen-binding proteins on the early evolution of multicellularity

Wong,

Bravo,

Yunker

et al. 2023

Preprint

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“…Globins are members of a broad group of oxygen-transport proteins, although their role as extracellular antigens is currently a matter of debate [41]. Globins functions might be specially striking as part of antigenic extracts from the host-parasite interface of trematodes.…”

Section: Resultsmentioning

confidence: 99%

Recognition Pattern of the Fasciola hepatica Excretome/Secretome during the Course of an Experimental Infection in Sheep by 2D Immunoproteomics

et al. 2021

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Excretory/secretory products released by helminth parasites have been widely studied for their diagnostic utility, immunomodulatory properties, as well as for their use as vaccines. Due to their location at the host/parasite interface, the characterization of parasite secretions is important to unravel the molecular interactions governing the relationships between helminth parasites and their hosts. In this study, the excretory/secretory products from adult worms of the trematode Fasciola hepatica (FhES) were employed in a combination of two-dimensional electrophoresis, immunoblot and mass spectrometry, to analyze the immune response elicited in sheep during the course of an experimental infection. Ten different immunogenic proteins from FhES recognized by serum samples from infected sheep at 4, 8, and/or 12 weeks post-infection were identified. Among these, different isoforms of cathepsin L and B, peroxiredoxin, calmodulin, or glutathione S-transferase were recognized from the beginning to the end of the experimental infection, suggesting their potential role as immunomodulatory antigens. Furthermore, four FhES proteins (C2H2-type domain-containing protein, ferritin, superoxide dismutase, and globin-3) were identified for the first time as non-immunogenic proteins. These results may help to further understand host/parasite relationships in fasciolosis, and to identify potential diagnostic molecules and drug target candidates of F. hepatica.

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“…Dps oxidizes Fe 2+ at its ferroxidase center and stores the resulting Fe 3+ within the iron core [ 82 ]. Hemerythrin (Hr) is a nonheme Fe-containing O 2 carrier-protein found in marine organisms [ 83 ]. Hr-like domain-containing proteins in prokaryotes are thought to perform secondary functions including O 2 sensing [ 84 ] and protecting from oxidative damage [ 85 ].…”

Section: Discussionmentioning

confidence: 99%

A Novel Marine Pathogen Isolated from Wild Cunners (Tautogolabrus adspersus): Comparative Genomics and Transcriptome Profiling of Pseudomonas sp. Strain J380

et al. 2021

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Cunner (Tautogolabrus adspersus) is a cleaner fish being considered for utilized in the North Atlantic salmon (Salmo salar) aquaculture industry to biocontrol sea lice infestations. However, bacterial diseases due to natural infections in wild cunners have yet to be described. This study reports the isolation of Pseudomonas sp. J380 from infected wild cunners and its phenotypic, genomic, and transcriptomic characterization. This Gram-negative motile rod-shaped bacterium showed a mesophilic (4–28 °C) and halotolerant growth. Under iron-limited conditions, Pseudomonas sp. J380 produced pyoverdine-type fluorescent siderophore. Koch’s postulates were verified in wild cunners by intraperitoneally (i.p.) injecting Pseudomonas sp. J380 at 4 × 103, 4 × 105, and 4 × 107 colony forming units (CFU)/dose. Host-range and comparative virulence were also investigated in lumpfish and Atlantic salmon i.p. injected with ~106 CFU/dose. Lumpfish were more susceptible compared to cunners, and Atlantic salmon was resistant to Pseudomonas sp. J380 infection. Cunner tissues were heavily colonized by Pseudomonas sp. J380 compared to lumpfish and Atlantic salmon suggesting that it might be an opportunistic pathogen in cunners. The genome of Pseudomonas sp. J380 was 6.26 megabases (Mb) with a guanine-cytosine (GC) content of 59.7%. Biochemical profiles, as well as comparative and phylogenomic analyses, suggested that Pseudomonas sp. J380 belongs to the P. fluorescens species complex. Transcriptome profiling under iron-limited vs. iron-enriched conditions identified 1159 differentially expressed genes (DEGs). Cellular metabolic processes, such as ribosomal and energy production, and protein synthesis, were impeded by iron limitation. In contrast, genes involved in environmental adaptation mechanisms including two-component systems, histidine catabolism, and redox balance were transcriptionally up-regulated. Furthermore, iron limitation triggered the differential expression of genes encoding proteins associated with iron homeostasis. As the first report on a bacterial infection in cunners, the current study provides an overview of a new marine pathogen, Pseudomonas sp. J380.

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Recent Insights into the Diversity and Evolution of Invertebrate Hemerythrins and Extracellular Globins

Cited by 3 publications

References 84 publications

Examining the role of oxygen-binding proteins on the early evolution of multicellularity

Examining the role of oxygen-binding proteins on the early evolution of multicellularity

Recognition Pattern of the Fasciola hepatica Excretome/Secretome during the Course of an Experimental Infection in Sheep by 2D Immunoproteomics

A Novel Marine Pathogen Isolated from Wild Cunners (Tautogolabrus adspersus): Comparative Genomics and Transcriptome Profiling of Pseudomonas sp. Strain J380

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