Enterobacter Species: Opportunistic Human and Plant Pathogens With Plant‐Beneficial Traits

Authors: Sara Jordan, Pieter de Maayer, Theo H. M. Smits, Teresa A. Coutinho

Abstract

Enterobacter species occur across diverse habitats and are best known for causing opportunistic and nosocomial infections in humans. The taxonomy of this genus is complex, with many species reassigned to and from this genus. Their interaction with plants is multifaceted. Strains of certain species cause opportunistic plant diseases.

Host Range

Enterobacter species affect a wide range of plant hosts.

Disease Symptoms

They cause a range of symptoms including leaf spots and blight, wilt and root diseases, decay and soft rot and cankers.

Plant‐Beneficial Traits

Some Enterobacter species include strains that are plant growth promoters and occur either in the rhizosphere or as endophytes. Additionally, some strains can protect their hosts from pathogen attack and are regarded as promising biological control agents. Some strains also have potential for the bioremediation of various compounds.

Genomic Features

Information on the pathogenicity and virulence mechanisms of plant‐pathogenic Enterobacter species is limited. Comparison of diverse genomic features revealed no overall differences between plant‐pathogenic and plant‐beneficial strains.

Conclusion

While often reported as a plant pathogen, there is currently no evidence that Enterobacter is the primary cause of any of the reported diseases. In many cases, they would rather act opportunistically. This remains a significant concern, as a wide range of hosts are affected, and problems may intensify due to global warming. It is crucial to investigate these strains for plant pathogenicity and evaluate the risks to human health.

Introduction

The family Enterobacteriaceae comprises gram‐negative, rod‐shaped, facultatively anaerobic bacteria (Adeolu et al. 2016). Although proposed in 1937, the family faced considerable controversy regarding its classification and type genus until it was validly published in the Approved Lists of Bacterial Names in 1980 (Farmer et al. 1980; Janda and Abbott 2021). In 2016, the family Enterobacteriaceae was split into seven new families within the novel order Enterobacterales, with Enterobacter as the type genus of the order. This separation led to the formation of Enterobacteriaceae fam. nov. from the “Enterobacter–Escherichia clade” with Escherichia as the type genus (Adeolu et al. 2016). Members of this family are ubiquitous and many are known pathogens, affecting humans, other animals and plants (Brenner and Farmer 2015). According to the List of Prokaryotic Names with Standing in Nomenclature, the family Enterobacteriaceae currently comprises 38 validly published genera including the genus Enterobacter (Meier‐Kolthoff et al. 2022).

The genus Enterobacter is best known as an opportunistic human pathogen (Coutinho et al. 2024; Davin‐Regli et al. 2019). Besides occurring as natural commensals in the gastrointestinal tracts of humans and other animals, they are commonly found in diverse terrestrial and aquatic environments. Species of Enterobacter have been isolated from water, sewage, soil, plants and even the International Space Station (Babalola et al. 2023; Biggel et al. 2022; Maguvu and Bezuidenhout 2021; Manter et al. 2011; Singh et al. 2018). Several Enterobacter species have been reported as plant pathogens (Grimont and Ageron 1989; Ji et al. 2022). On the other hand, some strains may play beneficial roles as plant growth‐promoting bacteria (PGPB) (Fadiji et al. 2023).

In this review, the environmental lifestyle of Enterobacter spp. is examined, including their taxonomy and roles as opportunistic human and plant pathogens, PGPB and biocontrol agents. New insights are provided by not only summarising previous findings but also re‐evaluating the taxonomy of earlier reports to clarify relevant species. In addition, comparative genomic analyses are integrated to explore genomic features linked to pathogenicity and plant‐beneficial traits. Through this approach, the current understanding of Enterobacter spp. as both plant‐associated pathogens and beneficial organisms is advanced and critical gaps for future research are identified.

Taxonomy

The genus Enterobacter was proposed in 1960 and encompassed two species, Enterobacter cloacae and Enterobacter aerogenes (Hormaeche and Edwards 1960). As taxonomic tools improved and more genera were described, species have been moved into and out of the genus. For example, Enterobacter sakazakii was moved to the genus Cronobacter (Iversen et al. 2008), while the Enterobacter agglomerans complex was separated into different species in the genus Pantoea, including Pantoea agglomerans (Gavini et al. 1989; Rezzonico et al. 2009).

Originally, species were described based solely on phenotypic and chemotaxonomic traits. Using these characteristics alone rarely allowed for the accurate identification of species due to their similarity in these traits (Mezzatesta et al. 2012). Later, commercial kits such as API 20E or Vitek 2 (BioMérieux) were used, but they were also unable to accurately discriminate between species (Davin‐Regli et al. 2019). The development and application of molecular techniques has led to considerable advancement in the ability to identify bacterial species in the family Enterobacteriaceae and genus Enterobacter. In combination with phenotypic and chemotaxonomic tests, the 16S rRNA gene sequence identity is commonly used to identify Enterobacter strains at the genus level. However, this gene is too conserved in the family Enterobacteriaceae to allow for the identification of strains at the genus and species level (Kämpfer 2012; Naum et al. 2008). Multilocus sequence analysis (MLSA) of four housekeeping genes proved to be more effective at species‐level delineation (Brady et al. 2013). The improvements in next‐generation sequencing (NGS) techniques for the generation of draft and complete genome sequences have brought about a reliable alternative to the identification techniques described above (Besser et al. 2018). Although the taxonomic assignment can be greatly improved, a drawback is that the genome databases still contain many genomes that were mislabelled in the past. A study using genome metrics determined that approximately three quarters of nearly 2000 genome sequences within the genus Enterobacter were not assigned to the correct species (Wu et al. 2020). The most recent studies, based on genomic metrics, recognised 30 described species within the genus Enterobacter, namely, E. adelaidei, E. asburiae , E. bugandensis, E. cancerogenus , E. chengduensis, E. chinensis, E. chuandaensis, E. cloacae , E. dissolvens , E. dykesii, E. hoffmannii , E. hormaechei , E. huaxiensis, E. kobei, E. ludwigii , E. mori , E. nematophilus, E. oligotrophicus, E. pasteurii, E. pseudoroggenkampii, E. quasihormaechei, E. quasimori, E. quasiroggenkampii, E. roggenkampii, E. rongchengensis, E. sichuanensis, E. soli , E. vonholyi, E. wuhouensis and E. xiangfangensis (He et al. 2024; Siderius et al. 2024).

A major challenge was that, due to the taxonomic changes, the identity of many Enterobacter spp. may not be reliable. For this reason, a re‐evaluation of the taxonomic position of the isolates was conducted for all studies cited in this review where possible. However, the taxonomically correct identity of some isolates could not be derived, either due to the lack of molecular data (previous identification only based on biochemical traits), or due to the inability to distinguish species or genera solely based on 16S rRNA gene sequences (Kämpfer 2012; Naum et al. 2008). The results of this re‐evaluation are indicated in the text and in the respective tables (Tables 1 and S1).

Enterobacter as Opportunistic Human Pathogen

The clinical importance of Enterobacter species lies in the fact that they are responsible for opportunistic and nosocomial human infections. While E. cloacae was previously regarded as the major human pathogen from this genus (Mezzatesta et al. 2012), genome analyses have shown that the most common Enterobacter species in clinical samples appears to be E. xiangfangensis (De Maayer et al. 2025; Wu et al. 2020). There are also reports of nosocomial outbreaks involving other species such as E. ludwigii and E. kobei (Manandhar et al. 2022; Schechner et al. 2021). E. bugandensis was described as one of the more aggressive Enterobacter species (Doijad et al. 2016; Falgenhauer et al. 2019), and model studies showed it to be as efficient as Salmonella enterica subsp. enterica serovar Typhimurium in inducing systemic infection (Pati et al. 2018).

A major concern with clinical Enterobacter isolates is that many of them are resistant to common antibiotics (Annavajhala et al. 2019; Singh et al. 2018). This trait is not limited to the genus Enterobacter but is also present within several other members of the family Enterobacteriaceae including the genera Escherichia, Klebsiella and Phytobacter (Ma et al. 2023; Sheppard et al. 2016; Smits et al. 2022). It is commonly based on the acquisition of mobile genetic elements containing several antibiotic resistance genes, mostly via so‐called multidrug plasmids (Arend et al. 2023; Dupouy et al. 2016; Weingarten et al. 2018). Treatment of bacteria that contain such plasmids may require the use of ‘last resort’ antibiotics, to which some bacteria have already developed resistance. For example, there is already a high prevalence of resistance to the ‘last resort’ antibiotic colistin in Enterobacter species in clinical strains (Fukuzawa et al. 2023; Liao et al. 2022).

Besides the use of antibiotics in human medication, their excessive use in livestock farming contributed to the development of antibiotic‐resistant bacteria (Mulchandani et al. 2023). These resistant bacteria can be transferred to humans through the consumption of contaminated food (McEwen and Collignon 2018). Antibiotics, along with antibiotic‐resistant bacteria and genes, may also transfer to agricultural soils through sewage sludge and animal manure, where they can colonise plants (Holden et al. 2009). When these plants are consumed, there is a risk of foodborne illnesses due to potential transmission to the human microbiome. Several studies have already reported colistin resistance in Enterobacter strains from livestock, environmental samples, wastewater and vegetables, highlighting the potential public health risk (Biggel et al. 2022; Lei et al. 2020; Moon et al. 2021; Xedzro et al. 2023).

Enterobacter Species as Opportunistic Plant Pathogens

Of the 30 currently described Enterobacter species, seven have been shown to be potential pathogens of a range of host plants, namely, E. asburiae , E. cancerogenus , E. cloacae , E. dissolvens , E. kobei , E. ludwigii , E. mori and E. quasiroggenkampii. In earlier “first reports” of a disease outbreak, the identification of the isolates to species level was based solely on chemotaxonomic traits and 16S rRNA gene sequence analyses. It is likely that the species may have been incorrectly identified (Table 1). Strains shown to cause wilt of mulberry trees identified as E. cloacae (Wang et al. 2008) were later recognised as E. mori (Zhu, Lou, et al. 2011). In many more recent reports, one to four additional housekeeping genes were sequenced, providing a more reliable identification of the causal agent. The whole genome sequence is only available for a few confirmed plant‐pathogenic strains (Table 1).

The number of reports describing new plant diseases caused by Enterobacter species has risen sharply in recent years. The first report of a plant‐pathogenic Enterobacter species was from a root disease of coconuts in 1976 (George et al. 1976). However, the causative agent of the disease was later described as being a phytoplasma (Ramjegathesh et al. 2012), and it may very well be that the isolated bacteria were part of the plant growth‐promoting rhizosphere population of the coconut tree (Indhuja et al. 2021). In the 1980s, there were reports of tree wetwood, internal yellowing in papaya and poplar canker disease. Since 2020, there have been 30 new reports of diseases ascribed to Enterobacter spp. Described symptoms include leaf spots and blight, wilt and root diseases, decay and soft rot and cankers (Figure 1).

In several cases, disease symptoms occurred when temperatures and relative humidity were high. Internal decay of onions was observed in California following a period of extreme heat (Bishop 1990), leaf rot on leaves of Odontioda occurred during summer with high air temperature (Takahashi et al. 1997), and diseased seedlings of pepper were only observed in greenhouses with relatively warm (36°C–38°C) and humid (80%–90% RH) conditions (García‐González et al. 2018).

Leaf Spots and Blight

Leaf symptoms caused by Enterobacter species begin as water‐soaked lesions, which become necrotic and are mostly surrounded by chlorotic halos. These symptoms were reported in cassava (Santana et al. 2012), chilli peppers (García‐González et al. 2018), Canna indica (Zhang et al. 2022), snake cucumber (Rady et al. 2022), strawberry (Ji et al. 2022), sorghum (Chen et al. 2023) and Coffea (Fang et al. 2024). Similar symptoms were observed on ginger, where multiple spots caused necrosis of the whole leaf (Tao et al. 2024). The causal agent in the outbreaks in cassava, chilli peppers and snake cucumber was reported to be E. cloacae , while re‐analysis indicated that they were E. hormaechei , E. ludwigii , or not identifiable on species level (Table 1). The disease in C. indica , sorghum and ginger was caused by E. mori , E. asburiae and E. quasiroggenkampii, respectively.

In rice, a range of symptoms was reported to be caused by Enterobacter species. In one case, the symptoms are described as spots on flag leaves, which were circular to elliptical with a white centre surrounded by irregular dark brown to black margins (Mirghasempour et al. 2022), while in another case, described symptoms included leaf yellowing, browning and withering (Cao et al. 2020, 2021). The causal agents in these two cases were identified as E. kobei and E. asburiae , respectively. In another report, E. asburiae was described to cause linear water‐soaked spots on rice leaf tips and margins, which became chlorotic and necrotic (Xue et al. 2021). However, the species assignment in these cases is not conclusive (Table 1).

In an outbreak in onions ascribed to Enterobacter, plants exhibited water‐soaking and leaf tip dieback as well as rot and splitting of the basal plates (Fallquist et al. 2007). These symptoms only occurred in areas that had a period of excessive soil moisture. The identity of the isolates could not be confirmed as no accession numbers of the 16S rRNA gene sequences were published.

Wilt and Root Diseases

Bacterial wilt symptoms typically result from root infections, with Ralstonia species usually identified as the causal agents (Peeters et al. 2013). In cases where Enterobacter species were found to cause wilt in mulberry, roots appeared wet and discoloured with brown lesions (Wang et al. 2008). Wilting that progresses from the bottom of the plant to the top distinguishes this disease from bacterial wilt caused by R. solanacearum (Wang et al. 2008). The causal agents were identified as E. mori and E. roggenkampii (Zhou et al. 2021; Zhu, Lou, et al. 2011). Furthermore, bacterial wilt has been reported in strawberry (Ji et al. 2022), tomato (Ning et al. 2024) and potato (Razanakoto et al. 2015), all caused by E. mori .

In the African marigold ( Tagetes erecta ), wilting linked to an E. cloacae isolate was a gradual process that differed from the symptoms that are caused by Ralstonia species (Jeevan et al. 2022). However, this pathogen could not be assigned to one of the existing Enterobacter species based on its 16S rRNA gene sequence (Table 1).

Decay and Soft Rot

Soft rot and/or decay symptoms of numerous plant species are typically caused by members of the family Pectobacteriaceae (Charkowski 2018). However, Enterobacter species have also been described to cause tissue maceration of bulbs, stems, rhizomes, corms and fruits.

In Allium species, internal bulb decay was observed, mainly during storage of the bulbs. This included onions (Bishop 1990), spring onions (shallots) (Asrul Arwiyanto et al. 2021) and garlic (Li et al. 2021). Although all have described the pathogen as E. cloacae , in the case of onions, the causal agent was identified as E. ludwigii while the re‐analysis showed that the spring onion pathogen might have been a Klebsiella sp. (Table 1), a genus that is also known to cause bulb diseases in onions (Liu et al. 2015). E. cloacae was also described as the causal agent of soft rot of Aloe vera , causing water‐soaked lesions on the leaves which later became yellow and rotted with the leaves collapsing at the base of the plant (Nguyen et al. 2021). Leaf rot of Ondontioda orchids was also described as being caused by E. cloacae (Takahashi et al. 1997), but this was solely base on biochemical identification.

In ginger, E. cloacae was described as an endophyte in healthy rhizomes, with symptoms of rot only becoming apparent in low‐oxygen/high‐moisture conditions (Nishijima et al. 2004). The organism causing rhizome soft rot was classified as E. cloacae (Zhao et al. 2022), but based on our analysis of the rpoB and gyrB sequences, this isolate should be identified as E. asburiae (Table 1).

Enterobacter hormaechei was reported to cause rot on dragon fruit (pitaya) stems (Retana‐Sánchez et al. 2019). The symptoms were described as small yellowish rot typically starting from the tips and outer edges of the stem and extending inward towards the stem, sometimes leading to the decay of the whole stem. Similar symptoms were also reported for E. cloacae (Masyahit et al. 2009; Soto et al. 2019), but here the submitted 16S rRNA sequence aligned better with Kosakonia, or the identification was unreliably based on biochemical identification (Table 1). Grey kernel rot of macadamia nuts was described as being caused by E. cloacae (Kaneshiro et al. 2003; Nishijima et al. 2007), but no gene sequences were available to confirm the identification. A strain isolated from ginger (B193‐3) also caused grey kernel rot in pathogenicity tests, while for the human isolate E. cloacae ATCC 13047 there were no significant differences from the controls inoculated with sterile distilled water (Nishijima et al. 2007). Low oxygen and high moisture levels promoted the development of the disease, similar to those conditions reported to contribute to ginger rhizome rot (Nishijima et al. 2004). In the case of soft rot of peaches, symptoms were observed on fruit in the orchard, which initially occurred as brown patches on the surface, with the fruit later rotting. The causal agent in this case was identified as E. mori (Ahmad et al. 2021). Further soft rot diseases were reported on potato and Mammillaria mystax , caused by E. kobei and E. dissolvens , respectively (Reyes‐García et al. 2020; Thanh et al. 2020). In soft rot/decay symptoms caused by Enterobacter species in peach and macadamia, an unpleasant odour was present (Ahmad et al. 2021; Nishijima et al. 2007), while the symptoms in onion and shallot were reported to be odourless or to have a slightly foul odour (Asrul Arwiyanto et al. 2021; Schwartz et al. 2008). Species of Enterobacter have also been reported to cause sprout decay of lucerne and cotton (Nagrale et al. 2020; Zhang and Nan 2013).

To confirm the pathogenicity of the isolated Enterobacter strains from decay and soft rot disease, a cell suspension was injected into the host plant for most studies. In the case of onion rot, other strains were tested, including the clinical E. cloacae type strain ATCC 13047, which showed similar symptom severities as the onion isolates (Bishop 1990). A study by Khanal and co‐workers used a “red scale assay” as an onion pathogenicity test, where surface‐sterilised red onion scales were punctured with a needle, and a small volume of cell suspension was placed on top of the wound. Out of 16 Enterobacter strains isolated from diseased onions, only two were found to be pathogenic using this assay, and compared to other organisms such as Burkholderia spp., they showed rather weak symptoms (Khanal et al. 2022).

There are other reports where Enterobacter was isolated from diseased plants, but these strains were later shown to be nonpathogenic, such as E. kobei ENHKU01 isolated from a diseased pepper plant (Liu et al. 2012). This indicates that in these cases, Enterobacter rather acts as an opportunist.

Cankers

There are only a few reports of Enterobacter strains causing cankers. E. cancerogenus was originally isolated from poplar tree cankers in 1966, where it was designated as Erwinia cancerogena (Dickey and Zumoff 1988). Today, this species is a well‐known clinical pathogen (Davin‐Regli et al. 2019). Canker‐like symptoms with bleeding from the vascular tissues were observed on kiwifruit vines, resulting in their death. The causal agent was identified as E. mori using genome sequencing (Zhang et al. 2021).

Genomic Features Related to Host Colonisation and Pathogenicity

There is limited information on the pathogenicity determinants present in Enterobacter species capable of infecting plants. However, it has been noted that bacterial pathogens employ similar strategies to colonise both plants and animals (Holden et al. 2013), and that there are shared factors involved in the pathogenesis of both plants and animals (Büttner and Bonas 2003; Rahme et al. 2000). Some traits are related to the virulence of human or plant pathogens, but also to plant growth promotion and biocontrol. Both beneficial and pathogenic bacteria can form biofilms, which help them colonise hosts. While biofilms containing beneficial bacteria can protect plants against biotic and abiotic stresses and promote plant growth, pathogenic biofilms can evade plant defence responses, leading to persistent infections and accelerated disease progression (Bogino et al. 2013; Danhorn and Fuqua 2007; Li, Narayanan, et al. 2024).

The presence of specific genes in Enterobacter strains with known growth‐promoting and biocontrol abilities has previously been reported (Guo et al. 2020; Ramakrishnan et al. 2023; Wang et al. 2022). However, only a few comparative genomic analyses, including a small number of genomes, have examined plant‐pathogenic and plant‐beneficial Enterobacter strains (Liu et al. 2013; Mustafa et al. 2020). To assess the relevance of the presence of reported genes for these traits, we analysed all available genomes of plant‐pathogenic Enterobacter strains as well as plant‐beneficial strains and compared them with all Enterobacter type strain genomes, which are mainly clinical isolates. Notably, the number of fully sequenced plant‐pathogenic Enterobacter genomes is very limited, with only four sequenced genomes that are currently available, compared to 14 genomes for Enterobacter strains reported as plant‐beneficial. Additionally, four plant‐beneficial strains that were erroneously assigned to the genus Enterobacter were also included together with the type strains of the actual species. Orthologous proteins were identified with Orthofinder v. 2.5.5 (Emms and Kelly 2019). Additionally, the presence of secretion systems was predicted using MacSyFinder v. 2.1.2 (Néron et al. 2022). The results of the comparative analyses are listed in Table S2 and summarised in Figure 2.

Fimbriae are widely distributed among the Pseudomonadota and are known to be critical for adhesion and the specific binding to tissues of preferred hosts. Liu and co‐workers identified 9–13 fimbrial protein‐encoding loci in different Enterobacter strains, four of which were conserved across all strains. These loci may allow them to colonise a wide range of hosts and environments (Liu et al. 2013).

Flagella play an important role in bacterial pathogenicity by providing motility and are also involved in other infection processes such as adhesion and biofilm formation (Chaban et al. 2015). It was previously reported that all Enterobacter strains contain a flag‐1 locus, encoding peritrichous flagella, in their genomes, while a few also have flag‐2 or flag‐3a loci (De Maayer et al. 2020), whose functions remain unknown. In our genome analyses, we identified several strains from different Enterobacter species that harbour either the flag‐2 or flag‐3a loci.

Biosynthetic genes for different extracellular polysaccharides (EPS) were common among all analysed genomes in this study. Genes responsible for the synthesis of colanic acid were present in all genomes, while biosynthesis genes for poly‐N‐acetyl‐glucosamine were lacking in a few strains. Other genes important for biofilm formation, such as genes responsible for cellulose biosynthesis (bcsEFG–bcs RQABZC) (Abidi et al. 2022) or curli fimbriae (csg BA–csg DEFG) (Kim et al. 2012), were also present in all analysed genomes.

Bacterial secretion systems are used by many pathogens to invade hosts, damage tissues and evade the immune system (Green and Mecsas 2016). Members of the genus Enterobacter possess several of the systems common in gram‐negative bacteria (Mustafa et al. 2020), namely the type I through type VI secretion systems (T1SS‐T6SS).

While the T3SS is a well‐known and important virulence factor in members of the order Enterobacterales causing soft‐rot disease (Charkowski et al. 2011), plant‐pathogenic strains of Enterobacter were reported to lack this secretion system (Zhang et al. 2021). Both T3SS and T4SS are not widely distributed in the genus Enterobacter. From the genomes analysed in this study, a T3SS was only detected in the type strain of E. pasteurii and T4SS in the type strains of E. quasimori and E. vonholyi. Genes encoding the other secretion systems T1SS, T2SS, T5SS and T6SS are abundant in the majority of the Enterobacter genomes. For E. cloacae, it was shown that two different T6SSs, named T6SS‐1 and T6SS‐2, are required for bacterial competition, cell adherence and gut colonisation in mice (Soria‐Bustos et al. 2020). Another type of T6SS (T6SS‐C) was recently described in Enterobacter, which was reported to be only abundant in E. cancerogenus (Peng et al. 2024).

Enterobacter Species as Plant‐Beneficial Organisms and Biocontrol Agents

In contrast to their pathogenic potential, there are numerous reports that Enterobacter species can be beneficial to plants, either as plant growth‐promoting bacteria (PGPB) or as biocontrol agents against various plant pests and pathogens. Additionally, members of the genus have also been described as phytoremediation agents (Figure 3). Several Enterobacter species have been reported to possess such traits, the majority of them identified as Enterobacter sp. or E. cloacae . However, re‐evaluation showed that in several cases, the described strain is not a member of the genus Enterobacter but rather belongs to the genera Klebsiella, Kosakonia, Leclercia, Lelliottia or Pseudescherichia. Confirmed Enterobacter strains were from the species E. adelaidei, E. asburiae , E. cancerogenus , E. cloacae , E. hormaechei , E. kobei , E. ludwigii , E. mori , E. roggenkampii and E. sichuanensis (Table S1).

Typically, PGPB or other plant‐beneficial bacteria are isolated from the rhizosphere (Ramesh et al. 2014), soil (Zuluaga et al. 2020), or as endophytes (Kumar and Dubey 2022). Some Enterobacter strains with plant‐beneficial traits have been isolated from extreme environments such as the desert (Andrés‐Barrao et al. 2017), semi‐desert (Ortega‐Ortega et al. 2024), or volcanic swamp (Shehata et al. 2017). Organisms from such environments have evolved to survive extreme conditions, resulting in a higher presence of genes associated with dormancy and stress response compared to those in non‐arid environments (Fierer et al. 2012).

Individual Enterobacter species and strains can have multiple growth‐promoting characteristics, and some have a dual function by also protecting their hosts from pathogen attack (Macedo‐Raygoza et al. 2019). Some PGPB additionally have the potential for bioremediation (Ali et al. 2020).

Nutrient Availability

Soil microorganisms are known to play a role in the acquisition of nutrients such as nitrogen and phosphorus by plants, especially in nutrient‐poor ecosystems (Van Der Heijden et al. 2008). Some Enterobacter species can mobilise insoluble phosphorus by solubilising inorganic phosphates such as hydroxyapatite and dicalcium phosphate (Abraham and Silambarasan 2015; Macedo‐Raygoza et al. 2019; Mahdi et al. 2020), or by mineralizing organic phosphorus such as phytate (Ramesh et al. 2014). The production of acetic, gluconic, lactic and malic acid was demonstrated for phosphate‐dissolving Enterobacter species (Suleman et al. 2018; Wang et al. 2022). The secretion of gluconic acid, mediated by the direct oxidation of glucose by the pyrroloquinoline quinone (PQQ)‐dependent glucose dehydrogenase (GDH), is a common mechanism for the solubilisation of mineral phosphate in several gram‐negative bacteria (Hantke and Friz 2022; Kim et al. 2003; Wagh et al. 2014). While the gdh gene was present in all compared Enterobacter genomes in this study, pqq genes were only found in the E. hormaechei complex and the closely related species E. quasihormaechei and E. pasteurii. In Escherichia coli , it was shown that strains unable to produce PQQ can excrete gluconic acid by using extracellular PQQ through the transporter PqqU (Hantke and Friz 2022). The pqqU gene encoding this transporter was found in all compared Enterobacter genomes in this study. Other gene clusters that were reported to be relevant for phosphorus availability, such as the phn and pho genes (Jacoby et al. 2017), were present in all genomes.

Several studies have reported the ability of Enterobacter spp. to fix nitrogen (Madhaiyan et al. 2013; Sajjad Mirza et al. 2001). Re‐evaluation of the identity of these reported strains revealed that some belong to the genera Klebsiella or Kosakonia (Table S1), which are known to possess this ability (Chen et al. 2020; Iniguez et al. 2004). Our analysis showed that nif genes are absent from most Enterobacter genomes, including all reported PGPB strains, but the genes are present in the genome of the E. chinensis type strain. Alternative nitrogen fixation (anf) genes or vanadium nitrogen fixation (vnf) genes are not present in any of the compared genomes.

In addition to phosphorus and nitrogen solubilisation, Enterobacter strains have also been reported to mobilise other trace elements such as potassium, calcium (Ranawat et al. 2021), zinc (Krithika and Balachandar 2016; Ullah et al. 2020) and with low solubilisation capacity, silicate (Cruz et al. 2022). Furthermore, soil inoculation with Enterobacter strain SRI‐229 led to enhancement of the mineral contents iron, zinc, copper, manganese and calcium in the harvested grains of chickpea and pigeon pea (Gopalakrishnan et al. 2016). It was hypothesised that this increase was due to the mobilising ability of siderophores produced by this strain.

Production of Plant Hormones

Some rhizobacteria are able to produce phytohormones such as auxins, cytokinins and gibberellins, which play key roles in plant development and defence responses (Egamberdieva et al. 2017; Spaepen et al. 2007; Vejan et al. 2016).

Indole‐3‐acetic acid (IAA) is an important plant hormone in the auxin class, and its production is the most frequently reported trait for growth promotion by Enterobacter strains (Table S1). Rhizobacteria can synthesise IAA from tryptophan using different pathways, but for Enterobacter, only the indole pyruvic acid (IPA) pathway was described (Duca and Glick 2020). While the genes of this pathway were reported as features of plant growth‐promoting Enterobacter spp. (Oh et al. 2018; Wang et al. 2022), the genome comparison in this study showed that these genes are widespread in all Enterobacter strains, including plant‐pathogenic and clinical isolates.

Gibberellins and cytokinins can be synthesised by some bacteria. Although this ability was not described for Enterobacter until a few years ago (Salazar‐Cerezo et al. 2018), gibberellic acid synthesis was recently reported in Enterobacter sp. WRS7, especially under osmotic stress conditions (Arora and Jha 2023). Currently, there is no genomic evidence for the synthesis of gibberellic acid and cytokinins in Enterobacter.

Abiotic Stress Tolerance

Drought and salinity are major abiotic stresses that impact plant growth. PGPB play a crucial role in helping plants cope with these stresses. Enterobacter species were shown to alleviate abiotic stresses such as drought and high soil salinity. In the presence of these bacteria, increases in plant growth, biomass and chlorophyll content were observed under stress conditions (Arora and Jha 2023; Pérez‐Rodriguez et al. 2022).

The degradation of the ethylene precursor 1‐aminocyclopropane‐1‐carboxylic acid (ACC) into ammonia and α‐ketobutyrate by the enzyme ACC deaminase is considered a key mechanism in helping plants cope with diverse stress conditions. This process reduces ethylene levels, thereby preventing growth inhibition and promoting root elongation, which enhances the ability of plants to withstand stress. Additionally, by lowering local ethylene concentrations, PGPB improve processes like nodulation and mycorrhizal colonisation, further supporting plant health (Ma et al. 2003). The strain E. cloacae UW4 was initially reported to possess the acdS gene encoding ACC deaminase, which was shown to be essential for its root elongation‐promoting effect (Li et al. 2000). However, this strain was later reclassified into the genus Pseudomonas (Duan et al. 2013). The acdS gene was not identified in members of the genus Enterobacter (Li et al. 2015), which was confirmed by the comparative genomics approach undertaken in this study.

Aside from the degradation of ACC, ethylene levels in plants can also be reduced through modulation of gene expression. For example, Enterobacter sp. C7 was shown to downregulate ethylene‐related genes in tomato plants, contributing to reduced ethylene accumulation under stress conditions (Ibort et al. 2018).

Halotolerant PGPB can accumulate osmoprotectants to balance osmotic pressure in cells, allowing survival under saline conditions. Inoculation with PGPB can increase the levels of these compatible osmolytes in plants, thereby alleviating the adverse effects of salt stress (Etesami and Glick 2020). For Enterobacter spp., there are reports of increased accumulation of soluble sugars and proline (Arora and Jha 2023; Pérez‐Rodriguez et al. 2022). The genes responsible for the synthesis of proline and trehalose were present in all compared genomes. Genes for glycine‐betaine biosynthesis, another important osmoprotectant, were identified from most genomes, but were not present in the genomes of E. soli and some strains outside the genus Enterobacter (Figure 2).

In addition, PGPB can enhance the antioxidant defence system in plants to reduce oxidative stress caused by salinity. This includes the upregulation of antioxidant enzymes, which help to scavenge reactive oxygen species (ROS) generated under stress conditions. For example, increased activities of superoxide dismutase, catalase and peroxidase were observed in wheat plants inoculated with E. cloacae ZNP‐4 (Singh et al. 2022). Furthermore, some Enterobacter strains may also indirectly alleviate abiotic stress by recruiting other beneficial microbes. For instance, E. ludwigii b3 was shown to mitigate drought stress in cultivated rice through both direct and indirect mechanisms, including modulation of the rhizosphere microbiome (Zhang et al. 2024).

Soil Remediation

There is increasing interest in phytoremediation, an approach where plants are used to absorb, degrade, or stabilise various chemical contaminants (Kafle et al. 2022; Yan et al. 2020). PGPB have been shown to enhance the phytoremediation of heavy metal contaminated soil (Yan et al. 2020). A review comparing the bioremediation potential of different genera found that Enterobacter and Klebsiella were the best candidates for soils contaminated with arsenic, cadmium and lead. These genera exhibited the highest levels of cadmium and lead tolerance, and they were also able to mitigate plant growth inhibition under phytotoxic metal concentrations (González Henao and Ghneim‐Herrera 2021).

The comparative genome analyses undertaken in this study showed that heavy‐metal resistance genes were widespread among all Enterobacter species. Arsenic and copper/silver resistance genes were detected in most of the genomes. The genomes of a few strains, primarily of clinical origin, additionally incorporated copper, chromate, mercury, nickel/cobalt and tellurium resistance genes (Figure 2).

In addition to promoting plant growth, Enterobacter species can improve heavy metal immobilisation by adsorbing metals to their cell walls, producing chelators and promoting precipitation processes. Enterobacter sp. YG‐14 was able to mobilise Fe–As complexes in mining soil by secreting the siderophore enterobactin and enhancing arsenic bioaccumulation in host plant roots (Chen et al. 2024). E. hormaechei DS02Eh01 was able to immobilise manganese via sorption, oxidation and pH‐induced precipitation (Li et al. 2022).

Apart from remediating heavy metals, some bacteria can also degrade certain organic soil pollutants. For example, Enterobacter strains were able to degrade the insecticides endosulfan (Abraham and Silambarasan 2015) and chlorpyrifos (Haque et al. 2022), the herbicide nicosulphuron (Xiao et al. 2025) and the analgesic acetaminophen (Pandey et al. 2025).

Furthermore, E. ludwigii strains were capable of alkane degradation, via a cytochrome P450 type‐alkane hydroxylase CYP153 (Yousaf et al. 2011). Among the strains compared in our study, the genomes of only five strains possessed a CYP153‐encoding gene, while three other genomes integrated an alkane monooxygenase gene.

Biocontrol Agents

Bacteria act as biocontrol agents by competing for nutrients and space, producing antimicrobial compounds and inducing plant defences (Legein et al. 2020; Whipps 2001). Enterobacter species have been shown to control the growth of several plant diseases caused by fungi, bacteria, oomycetes and nematodes (Table S1). These reported Enterobacter species include E. asburiae , E. cloacae , E. bugandensis, E. hormaechei , E. ludwigii and E. roggenkampii, and various mechanisms for biological control were described for these taxa.

Iron Competition

Bacteria that produce siderophores can protect plants by competing with pathogens for limited iron resources (Gu et al. 2020). Several Enterobacter strains with plant growth‐promoting traits were also capable of siderophore production (Table S1). For some of these strains, gene clusters for the synthesis and transport of enterobactin and aerobactin were reported to be present in the genomes (Cortés‐Albayay et al. 2024; Li, Gao, et al. 2024).

The comparative genomics approach employed in this study revealed that genes for enterobactin synthesis were present in all included genomes, whereas genes for aerobactin synthesis were present 90% of the Enterobacter genomes. Additionally, salmochelin genes are present in E. oligotrophicus CCA6, E. cancerogenus ATCC 33241^T^ and E. hormaechei subsp. steigerwaltii DSM 16691 and desferrioxamine E genes were present in E. soli .

A study by Gu et al. examined the ability of 2150 bacterial strains, including 378 Enterobacter isolates, to secrete siderophores and suppress the growth of the phytopathogenic bacterium Ralstonia solanacearum. The Enterobacter strains showed relatively high production of siderophores and siderophore‐mediated pathogen inhibition. Many of these strains were also able to protect tomato plants from infection (Gu et al. 2020).

Non‐Volatile Antimicrobial Agents

Some Enterobacter strains can inhibit the growth of phytopathogens by producing a broad array of antimicrobial agents. Enterobacter sp. EPR4 produces an extracellular chitinase that was able to inhibit the pathogenic fungus Sclerotinia sclerotiorum (Kumar et al. 2022). Furthermore, the purified chitinase of Enterobacter sp. KB3 was able to suppress growth of the pathogen Rhizoctonia solani (Velusamy and Kim 2011). Genes encoding a chitinase were present in 94% of the analysed genomes, with absence noted only in the species of E. asburiae , and were located in the vicinity of T2SS genes. In Burkholderia pseudomallei , it was shown that its chitinase activity is T2SS‐dependent (Burtnick et al. 2014), therefore it can be assumed that chitinase is also excreted by the T2SS in Enterobacter.

In addition to chitinases, other hydrolytic enzymes are considered a relevant mechanism in biocontrol bacteria (Riseh et al. 2024). Cellulase and protease activity have been demonstrated in several Enterobacter strains with reported antifungal or nematicidal properties (El‐Sayed et al. 2014; Saini et al. 2024). All genomes analysed in our study contained one to three genes annotated as cellulases. In contrast to chitinase there are no studies of purified proteases or cellulases from Enterobacter proving the biocontrol effect of these enzymes. However, for the strain E. asburiae HK169 it was shown that the nematicidal activity of the culture filtrate was reduced by a protease inhibitor, suggesting proteolytic enzymes contributed to the its nematicidal activity (Oh et al. 2018).

A peroxiredoxin ProV1 produced by an endophytic Enterobacter sp. was described to be effective against Verticillium dahliae (Zhang et al. 2020). Orthologous of the genes encoding of this peroxiredoxin were present in all analysed Enterobacter genomes.

Some strains that inhibited fungal growth also produced hydrogen cyanide (HCN), which was considered an antifungal metabolite (El‐Sayed et al. 2014; Fatima et al. 2022). In contrast, a study reported that the HCN levels produced by the rhizobacteria in vitro did not correlate with the observed biocontrol and that HCN rather acts as a growth‐promoting agent by increasing phosphate availability (Rijavec and Lapanje 2016). However, the hcnABC genes that encode HCN synthase (Laville et al. 1998) are not abundant in Enterobacter genomes.

Antimicrobial Volatile Organic Compounds

Volatile organic compounds (VOCs) produced by bacteria play a role in the control of plant pathogens (Tilocca et al. 2020). Several VOCs acting as biocontrol agents were reported for Enterobacter strains. For instance, 3‐methyl‐butanoic acid and 3‐methyl‐1‐butanol produced by Enterobacter sp. No. 26 and Enterobacter sp. No. 34 inhibited the growth of the rice pathogen Rhizoctonia solani (Wang et al. 2021), while 3‐methyl‐1‐butanol from Enterobacter strain TR1 showed potential as a postharvest biocontrol agent against Botrytis cinerea on tomato fruits (Chaouachi et al. 2021). The motility and biofilm formation of Agrobacterium tumefaciens in grapevine were inhibited by 9‐octadecenoic acid produced by Enterobacter sp. Ou80 (Etminani et al. 2022). Additionally, E. asburiae strain Vt‐7 produced phenylethyl alcohol and 1‐pentanol, which prevented the growth of Aspergillus flavus and aflatoxin production in peanuts in storage (Gong et al. 2019).

Induced Systemic Resistance

Aside from suppression of phytopathogens and pests, some Enterobacter strains have been reported to induce systemic resistance in their host plants (Mohamed et al. 2020). This mechanism, used by several biocontrol microorganisms, serves to trigger plant defence mechanisms, thereby, enhancing the ability of plants to fend off a wide range of pathogens and pests (Pieterse et al. 2014).

Induction of systemic resistance by E. cloacae PS14 was confirmed by an increased content of salicylic acid and increased peroxidase and lipoxygenase activities in potato plants (Mohamed et al. 2020). E. mori has the potential to produce the volatile organic compounds acetoin and 2,3‐butanediol (Zhang et al. 2021), which were reported to induce systemic resistance against plant pathogens as well as resistance to drought (Cho et al. 2008; Han et al. 2006). The bud genes responsible for biosynthesis of this VOC were present in all analysed genomes. On the other hand, these genes have been shown to be required for virulence in Pectobacterium carotovorum (Marquez‐Villavicencio et al. 2011).

Quorum Quenching

Another biocontrol mechanism reported for Enterobacter spp. is the disruption of quorum sensing in plant pathogens, although only a few studies have documented this to date. For example, an E. asburiae strain was shown to reduce the virulence of Dickeya species that are known as soft rot pathogens of various crops. This effect was attributed to the strain's ability to quench quorum‐sensing signals that regulate virulence factor expression (Liu et al. 2023).

The production of quorum‐quenching N‐acyl homoserine lactonase enzymes (AHL lactonases) has also been reported for Enterobacter sp. CS66 (Shastry et al. 2018). In our study, genes encoding AHL lactonases were detected exclusively in the species E. ludwigii .

Plant‐Beneficial Enterobacter spp.—From Lab to Field

Although Enterobacter species exhibit multiple plant growth‐promoting traits, these were primarily demonstrated in vitro or in controlled pot experiments. Field performance are far less predictable due to environmental stressors, variability and competition from native microbiota (Samonty et al. 2025). Only a few field studies have investigated Enterobacter‐based inoculants.

Positive effects on growth and yield were reported for chickpea and pigeon pea, but only one of seven strains in the study showed significant improvements among all evaluated promotion and yield traits (Gopalakrishnan et al. 2016). Furthermore an Enterobacter sp. strain alleviated salinity stress in pigeon pea under naturally saline conditions in the field (Anand et al. 2023). Another field trial reported that productivity of forage sorghum was slightly increased, but the increase was not significant compared to the control (Kaur et al. 2025). Biocontrol potential has also been demonstrated in field, such as suppression of Verticillium wilt, where one of two tested strains was efficient in the field despite both of them showing similar biocontrol activity in pot trials (Li et al. 2012). Another field trial showed that Enterobacter reduced Fusarium dry rot in potato, though its effect was lower than of Pseudomonas fluorescens while both were less effective than a treatment with the fungicide fludioxonil (Al‐Mughrabi 2010). These examples highlight that while Enterobacter shows promise as a plant‐beneficial organism, comprehensive field validation remains scarce and results from laboratory and pot experiments should be interpreted with caution.

Biosafety Considerations for Agricultural Applications

As several Enterobacter species are recognised opportunistic human pathogens, the use of Enterobacter strains as bio‐inoculants requires careful safety evaluation (Keswani et al. 2019). Only a few studies have assessed biosafety‐related traits in Enterobacter strains with plant‐beneficial characteristics. Some isolates have been tested on sheep blood agar and reported as haemolysis‐negative, including Enterobacter sp. DBA51 (Ortega‐Ortega et al. 2024), E. pseudoroggenkampii strain GVv1 (Taboadela‐Hernanz et al. 2025), and Enterobacter sp. MS32 (Suleman et al. 2018). A more comprehensive evaluation was performed in a recent study, where the plant growth‐promoting strain Enterobacter sp. JJG_Zn was additionally subjected to E. coli sensitivity tests and pathogenicity assays in albino mice, identifying this strain as potentially innocuous (Kaur et al. 2025). As such biosafety assessments remain rare and further genomic and phenotypic screening should accompany the development of Enterobacter‐based bio‐inoculants to ensure their safe use in agricultural systems.

Future Prospects

There has been a sharp increase in the number of “first reports” of plant diseases caused by Enterobacter species over the past decade (Figure 1). At the same time, the number of Enterobacter strains described as having plant beneficial traits has decreased. It is unclear whether this increase is due to a general rise in disease cases, or simply that the research focus has changed. However, climatic changes could also be a contributing factor to increased plant disease incidence, as some older cases were reported during periods of excessive temperatures (Bishop 1990; Takahashi et al. 1997). While this can cause stressful conditions for host plants, making them more vulnerable to attack by opportunistic pathogens, higher temperatures can also boost the growth of several bacteria, including Enterobacter.

The reports of phytopathogenic Enterobacter spp. show that they have a very broad host range; however, many reports are currently limited to individual cases. Multiple cases were reported for soft rot or decay of dragon fruit, ginger, onion and potato, for leaf spots or blight of rice and for wilt of mulberry.

The dearth of Enterobacter negative controls in plant pathogenicity assays in many of the reported plant disease makes it impossible to evaluate if only certain strains are pathogenic or if all member of a species or even the whole genus Enterobacter are opportunistic plant pathogens. In the case of internal onion decay, Enterobacter strains other than the isolates from diseased host plants were evaluated and showed comparable symptoms in the pathogenicity test (Bishop 1990). Furthermore, there was extensive variability between different trials, indicating a general problem of consistency in such pathogenicity assays, conceivably due to biological variations between host plants.

Many strains reported as plant pathogens or plant‐beneficial organisms have been misidentified, leading to a distorted picture of the importance of certain species. While E. cloacae was often described as a plant pathogen, re‐evaluation of their identities confirmed this species as the causal agent in only a few cases. Similar issues were previously reported for clinical strains. Many identifications were inconclusive due to reliance on 16S rRNA gene sequencing, highlighting the importance of more accurate identification methods such as MLSA or whole genome sequencing (WGS).

Furthermore, WGS is also important for gaining functional insights. Most studies have focused only on phenotypic analyses, with only a few including genome analyses. Although the number of studies incorporating genome sequencing increased in recent years, most have not conducted comprehensive comparisons of genotype and phenotype. More genomic information is needed for plant‐pathogenic strains, as there are currently only four strains with available genomes, which are all from different species and host plants. There are currently some inconsistencies between reported traits and the presence of known gene clusters (e.g., nif and hcn loci), which will need further investigation.

Several species of Enterobacter, including E. ludwigii , E. kobei and E. mori , have been reported to have both pathogenic and plant beneficial traits. From the current literature, it is not clear if reported PGPB or biocontrol strains can also act as opportunistic pathogens and vice versa.

We did not identify general differences in the genetic features that were commonly reported to be important for PGPB. This is best shown for the species E. ludwigii , for which the clinical type strain, the onion pathogen ECWSU1, the PGPB strain J49 and the biocontrol strain AA4 were included in the analysis. These strains showed no differences in the presence of most analysed features. The only difference is a flag‐3a locus that was restricted to the genome of the clinical E. ludwigii strain.

For the potential use of Enterobacter strains as PGPB, biocontrol, or remediation agents, it is crucial to thoroughly test these strains for plant pathogenicity and evaluate the risks to human health.

Author Contributions

Sara Jordan: investigation. Pieter de Maayer: writing – review and editing. Theo H. M. Smits: writing – review and editing, resources, project administration, funding acquisition, supervision. Teresa A. Coutinho: writing – original draft, writing – review and editing, funding acquisition, project administration.

Funding

This work was supported by Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung, SNSF210305588900.

Conflicts of Interest

The authors declare no conflicts of interest.

Supporting information