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Genome Note

A compilation of histidine kinase genes in Enterobacter hormaechei strain HCF3 isolated from the North West Province of South Africa

[version 1; peer review: 2 approved with reservations]
PUBLISHED 06 Dec 2024
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This article is included in the Genomics and Genetics gateway.

Abstract

This study investigates the histidine kinase (HK) gene repertoire of Enterobacter hormaechei strain HCF3, isolated from fresh cow dung in Mogosane Village, Northwest Province, South Africa. Histidine kinases are critical components of bacterial two-component signal transduction systems, enabling bacteria to sense and adapt to diverse environmental conditions. Given the growing concern over antimicrobial resistance (AMR) associated with E. hormaechei, this research elucidates the genetic components that facilitate its environmental adaptability.

After isolating the strain, genomic sequencing using Illumina technology, resulting in high-quality sequence data, was conducted. The assembled genome was meticulously annotated and deposited in the National Center for Biotechnology Information (NCBI) under BioProject number PRJNA991313, with additional accession numbers for raw reads (JAUOLV000000000.1) and BioSample (SAMN36292742). Histidine kinase genes were identified based on conserved domains, particularly HisKA and HATPase. This led to compiling a comprehensive HK gene catalogue with locus tags, protein accession numbers, and functional annotations.

To validate the HK gene set of E. hormaechei HCF3, we conducted a rigorous comparative analysis with other strains. This revealed that strain HCF1 contains 21 histidine kinase genes, HCF2 has 25, while HCF4 has 19. These findings underscore the diversity and conservation of HK genes across different Enterobacter species, providing a new perspective on their evolutionary significance.

The assembled dataset provides valuable insights into the signalling pathways of E. hormaechei, highlighting the potential roles of HKs in environmental sensing, adaptation, and pathogenicity. Furthermore, this research lays the groundwork for future studies on the applications of these genes in agriculture and biotechnology, offering new avenues for understanding and managing E. hormaechei in various ecological contexts.

Keywords

Enterobacter hormaechei, Histidine Kinase, Dataset, Genome, Plant pathogen, Cow dung

Introduction

It is well recognized that E. hormaechei can adapt to various ecological niches, such as soil, water, plants, and clinical settings. The bacteria are receiving more attention because of their association with antimicrobial resistance (AMR) and their significance in hospital-acquired illnesses. In North West Province in South Africa, E. hormaechei strain HCF3 was isolated from cow dung, providing an opportunity to investigate its genetic components, particularly those related to environmental sensing and adaptability.

Histidine kinases are essential components of bacterial two-component systems (TCS), that enable bacteria to detect environmental cues and modify gene expression in response. Cow dung and other manure-rich settings contain bacteria with competing microbial populations, fluctuating nutrient availability, and moisture fluctuations. Determining the histidine kinase genes in E. hormaechei HCF3 might help us understand how the bacterium endures these circumstances and whether or not these genes are involved in its pathogenicity and antibiotic resistance.

Essential sensor proteins in prokaryotes, histidine kinases (HKs), serve as receptors for stimuli such as mechanical stress, quorum-sensing molecules, and signals unique to certain plants, allowing bacteria to react to changes in their environment (Kabbara et al., 2019; Wang and Qian, 2019).

Crop improvement efforts rely heavily on HKs since they are essential to plants’ two-component systems (TCS), controlling development and environmental responses (Kenney, 2021). HKs are also used in industrial settings, to improve the synthesis of polyunsaturated fatty acids using genetic engineering (Hoang et al., 2021). Lembke and Carlson (2022) indicated that they are attractive targets for the development of antivirulence and antibiotics. In particular, suppressing Enterobacter hormaechei HKs may lessen the effects of the pathogen on plants. E. hormaechei enhances plant growth and development in crops such as tomatoes and okra by solubilizing vital macronutrients, such as phosphate and potassium. This increases biomass and improves plant architecture (Ranawat et al., 2021a, b); Roslan et al., 2020). According to Bendaha and Belaouni (2019), treated plants exhibit an enhanced fruit output and quality. It also improves the soil fertility, plant productivity, and crop quality. Furthermore, according to Pan et al. (2019), E. hormaechei encourages development without impairing anti-herbivore defense.

Although histidine kinases are essential, little information is available regarding these genes in E. hormaechei HCF3. Our work seeks to close this knowledge gap by assembling an extensive dataset of this HK genes in this strain. We discovered and annotated histidine kinase genes using genome sequencing and bioinformatics methods, offering information on their sequences and expected activities. Comparative investigations were carried out with different Enterobacter strains to further enhance our understanding of these genes and to identify commonalities and differences.

Therefore, this data provides the histidine kinase gene compilation of E. hormaechei HCF3, a valuable tool for scientists studying bacterial signalling pathways. A list of histidine kinase genes of E. hormaechei strain HCF3, whose complete genome sequence was published by Makhetha et al. (2023), was created. The dataset not only enhances our knowledge of E. hormaechei HCF3 but also serves as a foundation for future studies exploring the applications of these genes in agriculture and biotechnology.

Methodology

The genome sequences of 12 Enterobacter hormaechei strains HCF3 from faeces isolated from Fresh cow dung rectums samples from Mogosane Village in North West Province, South Africa (25°45′30.6″S 25°33′43.9″E) yielded E. hormaechei strain HCF3. The genome sizes ranged from 4.43 to 5.02Mb, with G + C contents of 55.5–56%, and contained 16–262 contigs. After cultivating the bacterial isolate Enterobacter hormaechei. The extracted DNA concentration was measured using a NanoDrop (ThermoFisher Scientific, Carlsbad, CA, USA), while DNA quality was evaluated using 2% agarose gel electrophoresis. The Illumina TruSeq DNA Nano Preparation Kit (Illumina, San Diego, CA, USA) was utilized to construct paired-end libraries with 2 × 150 bp reads. These libraries were subsequently sequenced on an Illumina Hiseq X platform, adhering to standard protocols at the Agricultural Research Council-Biotechnology Platform in South Africa. This procedure generated between 4,676,625 and 6,656,610 paired-end reads, each 2 × 150 bp in length. After quality-checking, the readings were combined together using SPAdes, annotated, and deposited in NCBI, as reported by Makhetha et al. (2023).

Thus, the genome sequence of the HCF3 strain of E. hormaechei, with BioProject number PRJNA991313 and raw reads under accession number JAUOLV000000000.1, BioSample number SAMN36292742, and GenBank assembly accession number GCA_022172285.1, were obtained. The genome sizes ranged from 4.43 to 5.02 Mb, and the G + C contents ranged from 55.5 to 56%. Conserved domains linked to HKs, specifically the HisKA (histidine kinase A) and HATPase domains, were used to identify histidine kinase genes. The histidine kinase gene catalogue was created by listing the genes with their characteristics, including locus tag, protein accession number, and annotation (shown in Table 1).

Table 1. Putative genes related to Histidine kinase characteristics in the genome of Enterobacter hormaechei strain HCF.

Putative GeneLocus Tag Go-Function Ncbi ProteinAnnotation
PhoQQYY53_01340phosphorelay sensor kinase activityMDO6164948.1 two-component system sensor histidine kinase PhoQ
RstBQYY53_02385phosphorelay sensor kinase activityMDO6165153.1 two-component system sensor histidine kinase RstB
NarXQYY53_05110phosphorelay sensor kinase activityMDO6165680.1 nitrate/nitrite two-component system sensor histidine kinase NarX
QYY53_06390MDO6165929.1 sensor histidine kinase
BaeSQYY53_06885phosphorelay sensor kinase activityMDO6166024.1 two-component system sensor histidine kinase BaeS
QYY53_07020MDO6166051.1 sensor histidine kinase
RcsCQYY53_07385phosphorelay sensor kinase activityMDO6166123.1 two-component system sensor histidine kinase RcsC
QYY53_07450MDO6166136.1 sensor histidine kinase
QYY53_07890MDO6166223.1 sensor histidine kinase
KdpDQYY53_08705phosphorelay sensor kinase activityMDO6166375.1 two-component system sensor histidine kinase KdpD
PhoRQYY53_10530phosphorelay sensor kinase activityMDO6166727.1 phosphate regulon sensor histidine kinase PhoR
NlpEQYY53_12705MDO6167152.1 envelope stress response activation lipoprotein NlpE
ArcBQYY53_13055phosphorelay sensor kinase activityMDO6167220.1 aerobic respiration two-component sensor histidine kinase ArcB
PmrBQYY53_13190MDO6167247.1 two-component system sensor histidine kinase PmrB
QseCQYY53_13925phosphorelay sensor kinase activityMDO6167388.1 quorum sensing histidine kinase QseC
QYY53_14080phosphorelay sensor kinase activityMDO6167419.1 hybrid sensor histidine kinase/response regulator."
QYY53_14105MDO6167423.1 sensor histidine kinase
QYY53_16870MDO6167961.1 ATP-binding protein
BarAQYY53_21340MDO6168841.1 two-component sensor histidine kinase BarA
EnvZQYY53_18125phosphorelay sensor kinase activityMDO6168207.1 two-component system sensor histidine kinase EnvZ
NarQQYY53_18570phosphorelay sensor kinase activityMDO6168296.1 "nitrate/nitrite two-component system sensor histidine kinase NarQ
QYY53_18755phosphorelay sensor kinase activityMDO6168333.1 HAMP domain-containing sensor histidine kinase
QseE/GlrKQYY53_19090phosphorelay sensor kinase activityMDO6168399.1 two-component system sensor histidine kinase QseE/GlrK."
CpxAQYY53_19480phosphorelay sensor kinase activityMDO6168476.1 envelope stress sensor histidine kinase CpxA
BarAQYY53_21340phosphorelay sensor kinase activityMDO6168841.1 two-component sensor histidine kinase BarA

Dataset validation

The discovered histidine kinase genes discovered from strain BD163 were compared with other Enterobacter genomes accessible in the NCBI database to confirm the histidine kinase gene set of E. hormaechei. This study aimed to investigate the diversity and conservation of histidine kinase genes in the Enterobacter genus. The histidine kinase genes of three Enterobacter strains (Enterobacter hormaechei HCF1, Enterobacter hormaechei HCF2, and Enterobacter hormaechei HCF4) were analyzed as part of a genome comparison study.

The methods described in the methodology section were followed to identify histidine kinase genes. Comparative analysis showed that, similar to strain HCF3, E. hormaechei HCF1 had 21 histidine kinase genes, and HCF2 strains each had 25 histidine kinase genes; however, strain HCF4 of E. hormaechei only had 19. These results show that different Enterobacter species have different frequencies of histidine kinase genes.

Authors contributions

Udeh EL: Data Curation, Methodology, Writing – Final Draft Preparation; Otun SO: Writing – Review & Editing and Makhetha L – Original Draft Preparation; Writing – Review & Editing; Ntushelo K: Conceptualization, Supervision, Writing – Review & Editing

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Udeh EL, Otun SO, Makhetha LLN and Ntushelo K. A compilation of histidine kinase genes in Enterobacter hormaechei strain HCF3 isolated from the North West Province of South Africa [version 1; peer review: 2 approved with reservations]. F1000Research 2024, 13:1493 (https://doi.org/10.12688/f1000research.157774.1)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Current Reviewer Status: ?
Key to Reviewer Statuses VIEW
ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 1
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PUBLISHED 06 Dec 2024
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Reviewer Report 27 Feb 2025
Angeliki Mavroidi, Department of Microbiology, Faculty of Medicine, General University Hospital of Patras, Patras, Greece 
Approved with Reservations
VIEWS 7
In the present study, the authors have performed whole genome sequencing (WGS) and predicted the histidine kinase (HK) gene repertoire of Enterobacter hormaechei strain HCF3,isolated from fresh cow dung in Mogosane Village, Northwest Province, South Africa. They have also performed comparative analysis histidine ... Continue reading
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Mavroidi A. Reviewer Report For: A compilation of histidine kinase genes in Enterobacter hormaechei strain HCF3 isolated from the North West Province of South Africa [version 1; peer review: 2 approved with reservations]. F1000Research 2024, 13:1493 (https://doi.org/10.5256/f1000research.173273.r365322)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Reviewer Report 10 Feb 2025
Reetika Debroy, Department of Biotechnology, Jaypee Institute of Information Technology, Noida, Uttar Pradesh, India 
Approved with Reservations
VIEWS 7
In the study “A compilation of histidine kinase genes in Enterobacter hormaechei strain HCF3 isolated from the North West Province of South Africa” by Udeh et al., the authors have made a comprehensive effort in investigating the histidine kinase (HK) gene repertoire ... Continue reading
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Debroy R. Reviewer Report For: A compilation of histidine kinase genes in Enterobacter hormaechei strain HCF3 isolated from the North West Province of South Africa [version 1; peer review: 2 approved with reservations]. F1000Research 2024, 13:1493 (https://doi.org/10.5256/f1000research.173273.r362390)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.

Comments on this article Comments (0)

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Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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