Biochemical and structural characterization of the cyanophage‐encoded phosphate‐binding protein: implications for enhanced phosphate uptake of infected cyanobacteria

Zhao, Fangxin; Lin, Xingqin; Cai, Kun; Jiang, Yong-Liang; Ni, Tianchi; Chen, Yue; Feng, Jianrong; Dang, Shangyu; Zhou, Cong‐Zhao; Zeng, Qinglu

doi:10.1111/1462-2920.16043

Cited by 12 publications

(5 citation statements)

References 66 publications

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“…Thus, it is likely that these PstS variants facilitate specific interaction with the cognate PstABC membrane bound components of the transport system of their preferred host (see also Zhao et al. [ 45 ]). In the six cases where pstS has not been acquired from the host genus, it is not clear what the host ranges of these phages are, and therefore, the interaction of these “incorrect” PstS types with their host’s PstABC requires further investigation.…”

Section: Resultsmentioning

confidence: 99%

Coordinated transcriptional response to environmental stress by a Synechococcus virus

Rihtman,

Torcello-Requena,

Mikhaylina

et al. 2024

The ISME Journal

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Viruses are a major control on populations of microbes. Often, their virulence is examined in controlled laboratory conditions. Yet, in nature, environmental conditions lead to changes in host physiology and fitness that may impart both costs and benefits on viral success. Phosphorus (P) is a major abiotic control on the marine cyanobacterium Synechococcus. Some viruses infecting Synechococcus have acquired, from their host, a gene encoding a P substrate binding protein (PstS), thought to improve virus replication under phosphate starvation. Yet, pstS is uncommon amongst cyanobacterial viruses. Thus, we asked how infections with viruses lacking PstS are affected by P scarcity. We show that production of infectious virus particles of such viruses is reduced in low P conditions. However, this reduction in progeny is not caused by impaired phage genome replication, thought to be a major sink for cellular phosphate. Instead, transcriptomic analysis showed that under low P conditions a PstS-lacking cyanophage increased the expression of a specific gene set that included mazG, hli2, and gp43 encoding a pyrophosphatase, a high-light inducible proteinand DNA polymerase respectively. Moreover, several of the upregulated genes were controlled by the hosts phoBR two-component system. We hypothesise that recycling and polymerization of nucleotides liberates free phosphate and thus allows viral morphogenesis, albeit at lower rates than when phosphate is replete or when phages encode pstS. Together, our data shows how phage genomes, lacking obvious P-stress related genes, have evolved to exploit their host’s environmental sensing mechanisms to coordinate their own gene expression in response to resource limitation.

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Section: Resultsmentioning

confidence: 99%

Coordinated transcriptional response to environmental stress by a Synechococcus virus

Rihtman,

Torcello-Requena,

Mikhaylina

et al. 2024

The ISME Journal

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“…5a). To date, only one provirus genome encoding PhnCDE was detected 73 , and the periplasmic high-affinity phosphate-binding gene pstS was the most commonly reported AMG related to phosphorus transport 74,75 . The viral phoR, phoB and phnC were expressed at varying levels, with the highest reaching up to 4.8…”

Section: Cold Seep Viruses Regulate Microbial Phosphorus Cycling Via ...mentioning

confidence: 99%

Illuminating microbial phosphorus cycling in deep-sea cold seep sediments using protein language models

Zhang,

He,

Wang

et al. 2024

Preprint

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Phosphorus is essential for life and critically influences marine productivity. Despite geochemical evidence of active phosphorus cycling in deep-sea cold seep ecosystems, the microbial processes involved remain poorly understood. Traditional sequence-based searches often fail to detect proteins with remote homology. To address this, we developed a protein language model (PLM) named LucaPCycle that integrates sequence and structural information. This PLM-based approach identified 4,606 new phosphorus-cycling protein families based on the non-redundant gene and genome catalogs from global cold seeps, substantially enhancing our understanding of their diversity, ecology, and function. Among previously unannotated sequences, we discovered three novel alkaline phosphatase families (ALP1, ALP2 and ALP3) that feature unique domain organizations and preserved enzymatic capabilities. These results highlight previously overlooked ecological importance of phosphorus cycling within cold seeps, corroborated by data from porewater geochemistry, metatranscriptomics, and metabolomics. We identified a previously unrecognized diversity of archaea contributing to organic phosphorus mineralization and inorganic phosphorus solubilization through various mechanisms. This includes ecologically significant groups such as Asgardarchaeota, anaerobic methanotrophic archaea (ANME), and Thermoproteota. Additionally, viruses can enhance their hosts' (e.g., ANME) phosphorus utilization through the PhoR-PhoB regulatory system and PhnCDE transporter, indirectly influencing methane dynamics. Overall, our PLM-based functional predictions are capable of accessing previously 'hidden' sequence spaces for microbial phosphorus cycling, and can be applied to other various ecosystems.

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“…To acquire phosphorus, cyanobacteria typically use an ABC-type phosphate transporter, consisting of a high affinity phosphate-binding protein (pstS) and two transmembrane proteins (pstC and pstA; Kamennaya et al, 2020). Studies have shown that the pstS gene in cyanophages can be effectively expressed during host infection and improve the phosphate uptake rate of the host after infection (Zhao et al, 2022), which may contribute to adaptation of the cyanophage to the oligotrophic environment. Coincide with our observation, pstS has been suggested to be one of the genes contributing to the difference in AMG content between coastal and open ocean phage isolates (Fuchsman et al, 2023).…”

Section: Large Numbers Of Amgs To Enhance the Fitness Of Nanhaivirus ...mentioning

confidence: 99%

Characterization and genomic analysis of an oceanic cyanophage infecting marine Synechococcus reveal a novel genus

et al. 2023

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Cyanophages play a crucial role in the biogeochemical cycles of aquatic ecosystems by affecting the population dynamics and community structure of cyanobacteria. In this study, a novel cyanophage, Nanhaivirus ms29, that infects Synechococcus sp. MW02 was isolated from the ocean basin in the South China Sea. It was identified as a T4-like phage using transmission electron microscopy. Phylogenetic analysis demonstrated that this cyanophage is distinct from other known T4-like cyanophage, belonging to a novel genus named Nanhaivirus within the family Kyanoviridae, according to the most recent classification proposed by the International Committee on Taxonomy of Viruses (ICTV). The genome of this novel cyanophage is composed of 178,866 bp of double-stranded DNA with a G + C content of 42.5%. It contains 217 potential open reading frames (ORFs) and 6 tRNAs. As many as 30 auxiliary metabolic genes (AMGs) were identified in the genome, which related to photosynthesis, carbon metabolism, nutrient uptake and stress tolerance, possibly reflecting a genomic adaption to the oligotrophic environment. Read-mapping analysis showed that Nanhaivirus ms29 mainly distributed in temperate and tropical epipelagic waters. This study enriches of the virus gene database of cyanophages and provides valuable insights into the phylogeny of cyanophages and their interactions with their hosts.

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Biochemical and structural characterization of the cyanophage‐encoded phosphate‐binding protein: implications for enhanced phosphate uptake of infected cyanobacteria

Cited by 12 publications

References 66 publications

Coordinated transcriptional response to environmental stress by a Synechococcus virus

Coordinated transcriptional response to environmental stress by a Synechococcus virus

Illuminating microbial phosphorus cycling in deep-sea cold seep sediments using protein language models

Characterization and genomic analysis of an oceanic cyanophage infecting marine Synechococcus reveal a novel genus

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