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International Journal for Parasitology: Parasites and Wildlife logoLink to International Journal for Parasitology: Parasites and Wildlife
. 2026 Jun 8;30:101248. doi: 10.1016/j.ijppaw.2026.101248

Molecular detection and characterization of hemotropic mycoplasma in long-tailed macaques (Macaca fascicularis) previously unreported in provinces in southern Thailand

Thanisorn Konlertvanich a, Supakarn Kaewchot b, Piya Sereerak b, Salintorn Thongsahuan b, Sakulchit Wichainchot c, Thanawat Hmaidee d, Wanat Sricharern a,e,⁎
PMCID: PMC13273680  PMID: 42318317

Abstract

Hemoplasmas are Gram-negative bacteria that can cause hemolytic anemia in a variety of mammalian species, including non-human primates. This study investigated the molecular prevalence and genetic characteristics of hemoplasmas in free-ranging long-tailed macaques in three previously unreported provinces in southern Thailand. In total, 210 blood samples were collected from long-tailed macaques in Phang Nga, Phetchaburi, and Satun provinces. DNA was extracted from the blood samples and screened for hemoplasmas using a broad-range nested polymerase chain reaction (PCR) assay targeting the 16S rRNA gene. Positive samples were sequenced for species identification, and phylogenetic analysis was performed to determine their genetic relationships. Overall, 35.7% (75/210; 95% CI = 29.2–42.6%) of the samples tested positive for hemoplasmas. Sequence analysis showed 99.3–100.0% identity with Candidatus Mycoplasma haematomacacae. Phylogenetic analysis confirmed that all sequences clustered within the Ca. M. haematomacacae clade, together with other reported isolates from macaques in several countries, including Thailand. In conclusion, this study has provided molecular evidence of Ca. M. haematomacacae infection in long-tailed macaques in areas where such infections had not been previously reported. Based on the results of this study, long-tailed macaques in various regions of Thailand might be infected with and act as reservoirs for this pathogen.

Keywords: Candidatus mycoplasma haematomacacae, Hemoplasmas, Long-tailed macaques, Macaca fascicularis, Thailand

Graphical abstract

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Highlights

  • •

    Molecular evidence of hemoplasmas in long-tailed macaques from newly reported areas.

  • •

    Ca. M. haematomacacae was identified by broad-range nested PCR targeting 16S rRNA.

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    Phylogenetic tree showed that sequences clustered in the Ca. M. haematomacacae clade.

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    Prevalence of 35.7% indicated potential hemoplasma transmission risk in the area.

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    Long-tailed macaques may act as hemoplasma reservoirs with potential spillover risk to humans.

1. Introduction

Hemotropic Mycoplasma species (hemoplasmas) are cell wall-less, Gram-negative, unculturable bacteria that adhere to the surface of mammalian erythrocytes (de Oliveira Battisti et al., 2024; Messick, 2004). These organisms bind to specific receptors on erythrocytes, leading to alterations of the red blood cell membrane and induction of programmed cell death (eryptosis) (Felder et al., 2011). Transmission occurs primarily through blood exposure or blood-sharing routes, thereby providing opportunities for hematophagous arthropods, including flies, midges, mosquitoes, ticks, and lice, to act as potential vectors (Arendt et al., 2024). Hemoplasmas can cause both acute and chronic infections in vertebrates, with acute infection possibly leading to severe and sometimes fatal hemolytic anemia, whereas chronic infection may range from asymptomatic to life-threatening, depending on host susceptibility (Willi et al., 2007). Host factors, such as age, underlying illness, and immune status, considerably influence both infection risk and disease severity (Messick, 2004; Willi et al., 2007).

Hemoplasmas have been reported in a broad range of mammalian hosts, including Mycoplasma haemocanis in dogs (Aktas and Ozubek, 2018), Mycoplasma haemofelis, Candidatus Mycoplasma haemominutum, and Candidatus Mycoplasma turicensis in cats (Aquino et al., 2014; Assarasakorn et al., 2012), Mycoplasma suis in pigs (Yuan et al., 2009), Mycoplasma spp. in rodents (Goncalves et al., 2015), Candidatus Mycoplasma hemohomonis in bats (Millan et al., 2015), and Candidatus Mycoplasma haemobos in cattle (de Mello et al., 2019). Additionally, several hemoplasma species have been reported among diverse wild animal populations, including opossums, rodents, and mongooses (Goncalves et al., 2020; Sharifiyazdi et al., 2014).

Non-human primates (NHPs) also constitute an important host group for hemoplasmas. Although hemoplasma infections in NHPs are generally considered subclinical and rarely associated with severe disease, infected animals may serve as reservoir hosts that contribute to pathogen maintenance and circulation within primate populations (Sricharern et al., 2021). Hemoplasma infections have been identified in various NHP species worldwide. Specifically, Candidatus Mycoplasma kahanei was detected in squirrel monkeys and howler monkeys in Brazil, with prevalences of 35.71% (35/98) and 26.47% (18/68), respectively (Bonato et al., 2015; de Melo et al., 2019). Furthermore, Candidatus Mycoplasma aoti was detected in owl monkeys (Aotus trivirgatus) in the United Kingdom (Barker et al., 2011), while Candidatus Mycoplasma haemomacaque (currently reclassified as Candidatus Mycoplasma haematomacacae) was identified in long-tailed macaques (Macaca fascicularis) in Thailand, with reported prevalences of 55.07% (125/227), 11.2% (38/339), and 59.64% (334/560) in previous studies (Narapakdeesakul et al., 2024; Sricharern et al., 2021; Suksai et al., 2019). Additionally, Ca. M. haematomacacae was detected in Assamese macaques (Macaca assamensis) in Thailand, with a reported prevalence of 17.3% (23/133) (Rucksaken et al., 2024).

Several species of macaques are present in Thailand: long-tailed macaques (M. fascicularis), pig-tailed macaques (Macaca nemestrina), stump-tailed macaques (Macaca arctoides), Assamese macaques (M. assamensis), Indochinese rhesus macaques (Macaca mulatta), and northern pig-tailed macaques (Macaca leonina) (Roos et al., 2014). Among these, long-tailed macaques are distributed widely throughout southern Thailand, where many groups inhabit areas in proximity to human communities. This overlap between macaque habitats and populated areas leads to frequent human-macaque interactions and facilitates shared environments (Malaivijitnond and Hamada, 2008; Schurer et al., 2019; Suwannarong et al., 2023).

Hemoplasmas are of growing zoonotic concern. Some studies have reported human infections caused by animal-origin hemoplasmas, including Candidatus Mycoplasma haematoparvum from dogs (Maggi et al., 2013a), Mycoplasma ovis from small ruminants (Sykes et al., 2010), and M. suis from pigs (Yuan et al., 2009). Considering that NHPs, particularly macaques, play an important role as reservoir hosts for various zoonotic pathogens (Schurer et al., 2019; Suwannarong et al., 2023), the presence of diverse hemoplasma species in macaques raises important questions regarding the potential for cross-species transmission. Although no confirmed cases of hemoplasma transmission from NHPs to humans have been reported to date, the close ecological interface between humans and macaques underscores the need for continued surveillance for zoonotic agents.

However, there has been limited reporting on the prevalence and molecular characteristics of hemoplasmas in long-tailed macaques in Thailand, with data restricted to several provinces in the central (Lop Buri, Samut Songkhram, and Samut Sakhon), southern (Phuket, Phatthalung, and Songkhla), western (Prachuap Khiri Khan), eastern (Chonburi), and northeastern (Amnat Charoen and Mukdahan) regions (Narapakdeesakul et al., 2024; Sricharern et al., 2021; Suksai et al., 2019). Although numerous provinces have not yet reported cases, many of them host NHP populations that frequently interact with humans, making it crucial to detect hemoplasmas in these areas. Thus, the present study aimed to determine the molecular prevalence of hemoplasmas in long-tailed macaques from understudied provinces in southern Thailand (Satun, Phang Nga, Phetchaburi). Additionally, this study aimed to perform genetic characterization and phylogenetic analysis of the detected hemoplasmas.

2. Materials and methods

2.1. Ethical statement

The protocols involving animal use in this research were approved by the Kasetsart University Institutional Animal Care and Use Committee (IACUC), Bangkok, Thailand, under the Ethical Review Board of the Office of the National Research Council of Thailand (NRCT) (Approval ID: ACKU67-VTN-001). This approval ensured the ethical conduct of all scientific research.

2.2. Study period and locations

Blood samples were collected from May 2023 to June 2024 from long-tailed macaques in three provinces of southern Thailand, namely Phetchaburi, Phang Nga, and Satun (Fig. 1). In these provinces, long-tailed macaques commonly inhabit areas located at the interface between urban communities and forest habitats, where they frequently enter residential areas and interact with the local residents. Laboratory analyses were conducted at the Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand.

Fig. 1.

Fig. 1

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Map of Thailand showing sampling sites for long-tailed macaques in Phetchaburi, Phang Nga, and Satun provinces (Modified from https://www.canva.com/).

2.3. Sample size and blood sample collection

The sample size was estimated using Epitools (https://epitools.ausvet.com.au) with an expected proportion of 0.17 based on previous study in Thailand (Rucksaken et al., 2024). The precision of the estimate and the confidence level were set as 5% and 95%, respectively. The calculated sample size was 217 samples. In this study, 210 blood samples were collected using a convenience sampling method from free-ranging long-tailed macaques in the study areas, comprising 71 samples (37 males and 34 females) from Ban Laem district, Phetchaburi province; 109 samples (61 males and 48 females) from Mueang Satun district, Satun province; and 30 samples (14 males and 16 females) from Mueang Phang Nga district, Phang Nga province. The macaques were humanely captured and initially sedated with xylazine hydrochloride (0.5–2 mg/kg body weight), followed by anesthesia with tiletamine-zolazepam (2–5 mg/kg body weight) (Hmaidee et al., 2025). Both drugs were administered via intramuscular injection in accordance with the approved protocol. Approximately 1 mL of blood was collected from the femoral vein of each monkey into tubes containing ethylenediaminetetraacetic acid (EDTA). Licensed veterinarians from the Department of National Parks, Wildlife, and Plant Conservation performed all procedures. The samples were kept cool during transportation to the laboratory and subsequently stored at −40°C before DNA extraction.

2.4. Molecular analysis

DNA was extracted from 200 μL of blood using a QIAamp® DNA Blood Mini Kit (QIAGEN; Hilden, Germany), following the manufacturer's instructions. The quality and concentration of the extracted DNA were assessed using a NanoDrop (Thermo Fisher Scientific; Waltham, MA, USA). Extracted DNA was stored at −40°C until further analysis.

A broad-range nested polymerase chain reaction (PCR) protocol based on the 16S rRNA gene, as described by Kaewmongkol et al. (2016), was used to amplify Mycoplasma spp. DNA using two sets of primers. The primer sequences for the primary PCR were V1-F (5′-AGAGTTTGATCCTGGCTCAG-3′) and V9-R (5′-GNTACCTTGTTACGACTT-3′), while the primer sequences for the secondary PCR were V3-F (5′-ACTCCTACGGGAGGCAGCAG-3′) and V6-R (5′-CGACAGCCATGCANCACCT-3′). DNA from Anaplasma platys was included as a positive control and distilled water as a negative control in each PCR assay. To reduce the risk of contamination, molecular analyses were performed separately for samples from each province. The PCR mixture for both primer pairs contained 1x PCR buffer, 2 mM MgCl2, 0.2 mM dNTPs, 1 μM of each primer, 0.04 U/μL Taq DNA polymerase, and 1 μL of DNA template (1:100 diluted primary PCR product), with the total volume adjusted to 25 μL with distilled water. The cycling conditions for the primary PCR were: 5 min denaturation at 95°C, followed by 40 cycles of 95°C for 1 min, 50°C for 1 min, and 72°C for 1 min, and a final extension of 72°C for 10 min. The expected length of the primary PCR product was 1400 bp. The secondary PCR cycling conditions were: 95°C for 5 min, followed by 45 cycles of 95°C for 1 min, 55°C for 45 s, and 72°C for 45 s, and a final extension of 72°C for 10 min. The expected length of the secondary PCR product was approximately 700 bp. The secondary PCR products were analyzed using electrophoresis on a 1.2% (w/v) agarose-TAE gel. All PCR-positive samples yielding amplicons of the expected size (700 bp) were submitted for DNA purification. Subsequently, the purified products were sequenced using the Sanger method (ATGC Co., Ltd.; Pathum Thani, Thailand). The sequences were compared with published sequences in the GenBank nucleotide database using the BLAST program of the National Center for Biotechnology Information.

2.5. Phylogenetic analysis

The partial nucleotide sequences of the 16S rRNA genes obtained from this study were aligned with reference sequences of hemoplasma species for comparison obtained from GenBank NCBI (http://www.ncbi.nlm.nih.gov/genbank) using the ClustalW software. The phylogenetic relationships among the hemoplasmas were inferred using the maximum likelihood method based on the Tamura-Nei model in the MEGA 12 software (https://www.megasoftware.net/). The datasets were generated using 1000 bootstrap replicates.

2.6. Statistical analysis

The statistical relationship between the positive results of hemoplasmas and sex or locations of long-tailed macaques was analyzed based on Pearson's chi-square test using GraphPad Prism 10 (GraphPad Software, San Diego, CA, USA). Statistical significance was tested at P < 0.05.

3. Results

In total, 210 blood samples were collected from long-tailed macaques in southern Thailand. Detection was performed using a nested PCR assay targeting a 700 bp fragment of the 16S rRNA gene (Fig. 2), revealing that 35.7% (75/210; 95% CI = 29.2–42.6%) of the sampled long-tailed macaques tested positive. The locations with the highest to lowest infection rates were Phetchaburi, Satun, and Phang Nga provinces with values of 36.6% (26/71; 95% CI = 25.5–48.9%), 35.8% (39/109; 95% CI = 26.8–45.5%), and 33.3% (10/30; 95% CI = 17.2–52.8%), respectively. The infection rate in male and female macaques was the same at 35.7% (40/112; 95% CI = 26.9–45.3%) and 35.7% (35/98; 95% CI = 26.3–46.0%), respectively (Table 1).

Fig. 2.

Fig. 2

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Agarose gel electrophoresis showing expected PCR amplicon at 700 bp (M = DNA marker, S1–S3 = unknown samples, P = positive control, N = negative control).

Table 1.

Prevalence and odds ratios of Ca. M. haematomacacae infections in long-tailed macaques from Southern Thailand.

Variable No. of animals % of positive samples (N) 95% CI of proportion OR 95% CI of OR P value
Gender
 Male 112 35.7 (40/112) 26.9–45.3 1 Reference
 Female 98 35.7 (35/98) 26.3–46.0 1 0.58–1.79 >0.999
Location
 Phang Nga 30 33.3 (10/30) 17.2–52.8 1 Reference
 Phetchaburi 71 36.6 (26/71) 25.5–48.9 1.16 0.47–2.96 0.823
 Satun 109 35.8 (39/109) 26.8–45.5 1.11 0.50–2.63 >0.999
Total 210 35.7 (75/210) 29.2–42.6
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Abbreviations: CI = confidence interval, OR = odds ratio.

Based on the nucleotide sequence analysis of the partial 16S rRNA sequences, all sequences were 99.3–100.0% identical to previously published sequences of Ca. M. haematomacacae from Japan in Japanese macaques (AB820288) and Thailand in Assamese and long-tailed macaques (MZ960002, MW040092, respectively) in the GenBank database. The nucleotide sequences of the 16S rRNA genes of hemoplasmas from long-tailed macaques in the present study were submitted to the GenBank database under the accession numbers PX998692–PX998766.

The phylogenetic analysis revealed that all sequences obtained in the present study clustered within the same clade as Ca. M. haematomacacae identified in rhesus macaques (MK192131), long-tailed macaques (MW040088 and MK192130), and Assamese macaques (MZ960020) from Thailand, cynomolgus macaques (KC512401) from the United States, and Japanese macaques (AB820288) from Japan (Fig. 3).

Fig. 3.

Fig. 3

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Phylogenetic tree based on 16S rRNA gene sequences of the Mycoplasma genus produced using the maximum likelihood method, where sequences detected in current study shown as black circles (●).

A thorough statistical analysis was performed to assess the correlations between hemoplasma infection and the geographical location or gender of the long-tailed macaques. The odds ratios (ORs) of the positive samples from Phetchaburi (OR = 1.16, 95% CI = 0.47–2.96, p = 0.823) and Satun (OR = 1.11, 95% CI = 0.50–2.63, p > 0.999) were not significantly different from those of Phang Nga. The OR of gender in the samples from female macaques did not differ significantly from that of male macaques (OR = 1.00, 95% CI = 0.58–1.79, p > 0.999). Furthermore, there was no significant correlation between hemoplasma infection and the gender or location of the long-tailed macaques (Table 1).

4. Discussion

The present study identified evidence of Ca. M. haematomacacae in free-ranging long-tailed macaques in Phang Nga, Phetchaburi, and Satun provinces of southern Thailand. This species was selected for study because long-tailed macaques are the most widely distributed and commonly encountered macaque species in Thailand, frequently inhabiting areas in close proximity to human communities (Malaivijitnond and Hamada, 2008). These findings are consistent with other studies that reported this species in long-tailed macaques from other southern provinces, such as Phatthalung, Songkhla, Surat Thani, Nakhon Si Thammarat, Krabi, Phuket, and Narathiwat (Narapakdeesakul et al., 2024; Suksai et al., 2019). In addition, Ca. M. haematomacacae has been reported in other macaque species, including rhesus macaques (Suksai et al., 2019), pig-tailed macaques (Narapakdeesakul et al., 2024), and Assamese macaques (Rucksaken et al., 2024).

The prevalence of Ca. M. haematomacacae infection in long-tailed macaques in the present study was 35.7%, which was higher than those reported in other studies in Thailand, such as 17.3% (23/133) in Assamese macaques (Rucksaken et al., 2024), 11.2% (38/339) in long-tailed macaques (Sricharern et al., 2021), and 20.0% (4/20) in pig-tailed macaques (Narapakdeesakul et al., 2024). In addition, this prevalence was lower than those reported for the 55.1% (125/227) in long-tailed macaques and 65.7% (23/35) in rhesus macaques (Suksai et al., 2019) in Thailand, the 100% (9/9) in Japanese macaques in Japan (Sashida et al., 2014), and the 84.6% (44/52) in long-tailed macaques in the United States (Maggi et al., 2013b).

As no obvious clinical signs are commonly observed in hemoplasma-infected macaques, these infected animals may serve as important reservoir hosts for Ca. M. haematomacacae. Therefore, even in the absence of severe health effects or mortality, they could contribute to the maintenance and circulation of this organism within macaque populations and potentially other susceptible hosts.

The results of the present study indicated no significant differences in hemoplasma prevalence associated with the gender or location of the macaques. However, Suksai et al. (2019) indicated that the prevalence of hemoplasma infection in female long-tailed macaques exceeded that in male long-tailed macaques in Thailand. In contrast, a higher prevalence of hemoplasma infection in male macaques was observed in NHPs in Brazil, which might result from the aggressive behavior of male animals that facilitated transmission (Cubilla et al., 2017).

Phylogenetic analysis revealed that the 16S rRNA sequences detected in the long-tailed macaques in the present study clustered within the Ca. M. haematomacacae clade. This group was closely related to the sequences detected in Japanese macaques in Japan (Sashida et al., 2014), as well as Assamese macaques (Rucksaken et al., 2024), long-tailed macaques (Sricharern et al., 2021), and rhesus macaques (Suksai et al., 2019) in Thailand. Furthermore, a wide range of hemoplasma species has been identified in diverse NHP hosts across multiple geographic regions, such as Ca. M. kahanei, which has been observed in squirrel monkeys and howler monkeys (Bonato et al., 2015; de Melo et al., 2019), and Ca. M. aoti in owl monkeys (Barker et al., 2011).

Sequence alignment based on the 16S rRNA gene sequences revealed that Ca. M. haematomacacae detected in the present study showed no sequence variation among samples obtained from the three studied provinces, namely Phang Nga, Phetchaburi, and Satun. Furthermore, comparison with previously reported Ca. M. haematomacacae sequences from other provinces in Thailand (Rucksaken et al., 2024; Sricharern et al., 2021; Suksai et al., 2019) demonstrated a high degree of sequence conservation, with no nucleotide differences observed among Thai isolates. In addition, comparison with related sequences reported from other Asian countries, such as Japan (Sashida et al., 2014), revealed only a few nucleotide differences. These findings suggest that the 16S rRNA gene of Ca. M. haematomacacae is highly conserved across geographic regions and host populations, indicating relatively low genetic diversity among currently available sequences.

Based on the results of the present study, long-tailed macaques living in nearby communities could have a relatively high prevalence of Ca. M. haematomacacae infection. However, no infection has been reported in humans due to limited diagnostic investigations for this organism, particularly those based on molecular detection methods, thereby highlighting an important knowledge gap regarding its occurrence in humans. Other studies have reported the identification of hemoplasma infections in various animal species capable of transmitting to humans, including M. haemofelis-like species in Brazil, M. suis in China, M. ovis in Texas, The United States, and Ca. M. haematoparvum in Ireland and South Africa (dos Santos et al., 2008; Maggi et al., 2013c; Sykes et al., 2010; Yuan et al., 2009). The occurrence of the same infective hemoplasma species across many hosts indicates potential transmission to other species.

While the transmission pathways of hemoplasma in NHPs are not well-defined, prior investigations have identified hemoplasma DNA in Amblyomma spp. and lice originating from rats (Goncalves et al., 2020), fleas originating from goats (Ghauri et al., 2024), and arthropods originating from cattle, goats, sheep, and pigs (Arendt et al., 2024). These findings suggest that such arthropods may play a potential role as transmission vectors in NHPs. However, few studies have delineated the vectors of hemoplasmas in NHPs. Consequently, further epidemiological investigations are needed to identify potential reservoirs and vectors of hemoplasmas in Thailand. In addition, future studies should include surveillance in captive monkeys and other NHP species across different regions to better understand the transmission dynamics of these pathogens.

The limitations of this study should be acknowledged. First, molecular detection and phylogenetic analysis were based on a single genetic marker, the 16S rRNA gene, which may limit the resolution for evaluating genetic diversity among Ca. M. haematomacacae isolates. Second, clinical evaluations and hematological examinations were not performed in the sampled macaques; therefore, the association between hemoplasma infection and possible health effects could not be determined. In addition, potential arthropod vectors were not investigated for the presence of hemoplasmas, and humans living in the sampling areas were not examined for infection. Consequently, these identified limitations underscore critical knowledge gaps that should be systematically addressed in future investigations to provide a more comprehensive understanding of hemoplasma epidemiology and its potential zoonotic implications.

5. Conclusion

The present study provided molecular evidence of Ca. M. haematomacacae infection in long-tailed macaques from areas where such infections had not been previously reported (Phetchaburi, Satun, and Phang Nga provinces) in Thailand. Future studies should investigate hemoplasmas in diverse NHPs across different regions of Thailand, including human populations sharing the same habitats, to better understand the transmission dynamics and potential zoonotic risk to humans.

Data availability statement

The partial 16S rRNA sequences of ‘Candidatus Mycoplasma haematomacacae’ obtained in this study were deposited in the GenBank™ database (https://www.ncbi.nlm.nih.gov/nuccore) under the accession numbers PX998692–PX998766.

Declaration of generative AI and AI-assisted technologies in the writing process

During the preparation of this manuscript the authors used ChatGPT (developed by OpenAI) to assist with language and grammar guidance. After using this tool, the authors reviewed and edited the content as needed and take full responsibility for the content of the publication.

CRediT authorship contribution statement

Thanisorn Konlertvanich: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft, Writing – review & editing. Supakarn Kaewchot: Methodology, Resources. Piya Sereerak: Methodology, Resources. Salintorn Thongsahuan: Methodology, Resources. Sakulchit Wichainchot: Methodology. Thanawat Hmaidee: Methodology. Wanat Sricharern: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – review & editing.

Conflict of interest

The authors declare no conflicts of interest.

Acknowledgments

The Kasetsart University Research and Development Institute (KURDI), Bangkok, Thailand provided financial support. The Faculty of Veterinary Technology, Kasetsart University, Bangkok, Thailand, provided laboratory facilities and technical support. The veterinarians from the Department of National Parks, Wildlife and Plant Conservation, Ministry of Natural Resources and Environment were especially valuable for their assistance in sample collection.

References

  1. Aktas M., Ozubek S. A molecular survey of hemoplasmas in domestic dogs from Turkey. Vet. Microbiol. 2018;221:94–97. doi: 10.1016/j.vetmic.2018.06.004. [DOI] [PubMed] [Google Scholar]
  2. Aquino L.C., Hicks C.A., Scalon M.C., Lima M.G., Lemos Mdos S., Paludo G.R., Helps C.R., Tasker S. Prevalence and phylogenetic analysis of haemoplasmas from cats infected with multiple species. J. Microbiol. Methods. 2014;107:189–196. doi: 10.1016/j.mimet.2014.10.013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arendt M., Stadler J., Ritzmann M., Ade J., Hoelzle K., Hoelzle L.E. Hemotrophic mycoplasmas-vector transmission in livestock. Microorganisms. 2024;12(7) doi: 10.3390/microorganisms12071278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Assarasakorn S., Veir J.K., Hawley J.R., Brewer M.M., Morris A.K., Hill A.E., Lappin M.R. Prevalence of Bartonella species, hemoplasmas, and Rickettsia felis DNA in blood and fleas of cats in Bangkok, Thailand. Res. Vet. Sci. 2012;93(3):1213–1216. doi: 10.1016/j.rvsc.2012.03.015. [DOI] [PubMed] [Google Scholar]
  5. Barker E.N., Helps C.R., Neimark H., Peters I.R., Peters W., Tasker S. A novel haemoplasma species identified in archived primate blood smears. Vet. Microbiol. 2011;149(3–4):478–481. doi: 10.1016/j.vetmic.2010.11.016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bonato L., Figueiredo M.A., Goncalves L.R., Machado R.Z., Andre M.R. Occurrence and molecular characterization of Bartonella spp. and hemoplasmas in neotropical primates from Brazilian Amazon. Comp. Immunol. Microbiol. Infect. Dis. 2015;42:15–20. doi: 10.1016/j.cimid.2015.09.001. [DOI] [PubMed] [Google Scholar]
  7. Cubilla M.P., Santos L.C., de Moraes W., Cubas Z.S., Leutenegger C.M., Estrada M., Vieira R.F.C., Soares M.J., Lindsay L.L., Sykes J.E., Biondo A.W. Occurrence of hemotropic mycoplasmas in non-human primates (Alouatta caraya, Sapajus nigritus and Callithrix jacchus) of southern Brazil. Comp. Immunol. Microbiol. Infect. Dis. 2017;52:6–13. doi: 10.1016/j.cimid.2017.05.002. [DOI] [PubMed] [Google Scholar]
  8. de Mello V.V.C., de Souza Ramos I.A., Herrera H.M., Mendes N.S., Calchi A.C., Campos J.B.V., Macedo G.C., Alves J.V.A., Machado R.Z., Andre M.R. Occurrence and genetic diversity of hemoplasmas in beef cattle from the Brazilian Pantanal, an endemic area for bovine trypanosomiasis in South America. Comp. Immunol. Microbiol. Infect. Dis. 2019;66 doi: 10.1016/j.cimid.2019.101337. [DOI] [PubMed] [Google Scholar]
  9. de Melo C.M.F., Daneze E.R., Mendes N.S., de Souza Ramos I.A., Morales-Donoso J.A., Fernandes S.J., Machado R.Z., Andre M.R., da Rosa Sobreira M.F. Genetic diversity and hematological and biochemical alterations in Alouatta primates naturally infected with hemoplasmas in Brazil. Comp. Immunol. Microbiol. Infect. Dis. 2019;63:104–111. doi: 10.1016/j.cimid.2019.01.011. [DOI] [PubMed] [Google Scholar]
  10. de Oliveira Battisti L., Mongruel A.C.B., Fagundes-Moreira R., Baggio-Souza V., de Souza V.K., de Amorim D.B., Wagner P.G.C., Souza U.A., Goncalves A.P., Girotto-Soares A., de Faria Valle S., Andre M.R., Soares J.F. Post-mortem detection of hemoplasmas (hemotropic Mycoplasma spp.) in South American fur seal (Arctocephalus australis) sampled in Rio Grande do Sul State, southern Brazil. Comp. Immunol. Microbiol. Infect. Dis. 2024;109 doi: 10.1016/j.cimid.2024.102187. [DOI] [PubMed] [Google Scholar]
  11. dos Santos A.P., dos Santos R.P., Biondo A.W., Dora J.M., Goldani L.Z., de Oliveira S.T., de Sa Guimaraes A.M., Timenetsky J., de Morais H.A., Gonzalez F.H., Messick J.B. Hemoplasma infection in HIV-positive patient, Brazil. Emerg. Infect. Dis. 2008;14(12):1922–1924. doi: 10.3201/eid1412.080964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Felder K.M., Hoelzle K., Ritzmann M., Kilchling T., Schiele D., Heinritzi K., Groebel K., Hoelzle L.E. Hemotrophic mycoplasmas induce programmed cell death in red blood cells. Cell. Physiol. Biochem. 2011;27(5):557–564. doi: 10.1159/000329957. [DOI] [PubMed] [Google Scholar]
  13. Ghauri M.S.Z., Soomro S., Novianto D., Arnuphapprasert A., Kaewthamasorn M. Molecular detection and genetic characterization of hemotropic mycoplasmas in goats and fleas from Thailand. Sci. Rep. 2024;14(1) doi: 10.1038/s41598-024-81525-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Goncalves L.R., Herrera H.M., Nantes W.A.G., Santos F.M., Porfirio G.E.O., Barreto W.T.G., de Macedo G.C., Assis W.O., Campos J.B.V., da Silva T.M.V., Mariano L.C., Barros-Battesti D.M., Machado R.Z., Andre M.R. Genetic diversity and lack of molecular evidence for hemoplasma cross-species transmission between wild and synanthropic mammals from Central-Western Brazil. Acta Trop. 2020;203 doi: 10.1016/j.actatropica.2019.105303. [DOI] [PubMed] [Google Scholar]
  15. Goncalves L.R., Roque A.L., Matos C.A., Fernandes Sde J., Olmos I.D., Machado R.Z., Andre M.R. Diversity and molecular characterization of novel hemoplasmas infecting wild rodents from different Brazilian biomes. Comp. Immunol. Microbiol. Infect. Dis. 2015;43:50–56. doi: 10.1016/j.cimid.2015.10.006. [DOI] [PubMed] [Google Scholar]
  16. Hmaidee T., Rucksaken R., Kaewchot S., Sereerak P., Thongsahuan S., Jarudecha T., Wichainchot S., Wilaisri P., Thabthimsri C., Premphoolsawat P., Sricharern W. Molecular prevalence and identification of zoonotic plasmodium spp., including Plasmodium knowlesi, Plasmodium cynomolgi, and Plasmodium inui, in long-tailed macaques (Macaca fascicularis) of southern Thailand. Vet. Med. Int. 2025;2025 doi: 10.1155/vmi/3024193. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kaewmongkol G., Maneesaay P., Suwanna N., Tiraphut B., Krajarngjang T., Chouybumrung A., Kaewmongkol S., Sirinarumitr T., Jittapalapong S., Fenwick S.G. First detection of ehrlichia canis in cerebrospinal fluid from a nonthrombocytopenic dog with meningoencephalitis by broad-range PCR. J. Vet. Intern. Med. 2016;30(1):255–259. doi: 10.1111/jvim.13788. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maggi R.G., Compton S.M., Trull C.L., Mascarelli P.E., Mozayeni B.R., Breitschwerdt E.B. Infection with hemotropic mycoplasma species in patients with or without extensive arthropod or animal contact. J. Clin. Microbiol. 2013;51(10):3237–3241. doi: 10.1128/JCM.01125-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Maggi R.G., Mascarelli P.E., Balakrishnan N., Rohde C.M., Kelly C.M., Ramaiah L., Leach M.W., Breitschwerdt E.B. "Candidatus Mycoplasma haemomacaque" and Bartonella quintana bacteremia in cynomolgus monkeys. J. Clin. Microbiol. 2013;51(5):1408–1411. doi: 10.1128/JCM.03019-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maggi R.G., Mascarelli P.E., Havenga L.N., Naidoo V., Breitschwerdt E.B. Co-infection with Anaplasma platys, Bartonella henselae and Candidatus Mycoplasma haematoparvum in a veterinarian. Parasites Vectors. 2013;6:103. doi: 10.1186/1756-3305-6-103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Malaivijitnond S., Hamada Y. Current situation and status of long-tailed macaques (Macaca fascicularis) in Thailand. Nat. Hist. J. Chulalongkorn Univ. 2008;8(2):185–204. [Google Scholar]
  22. Messick J.B. Hemotrophic mycoplasmas (hemoplasmas): a review and new insights into pathogenic potential. Vet. Clin. Pathol. 2004;33(1):2–13. doi: 10.1111/j.1939-165x.2004.tb00342.x. [DOI] [PubMed] [Google Scholar]
  23. Millan J., Lopez-Roig M., Delicado V., Serra-Cobo J., Esperon F. Widespread infection with hemotropic mycoplasmas in bats in Spain, including a hemoplasma closely related to "Candidatus Mycoplasma hemohominis". Comp. Immunol. Microbiol. Infect. Dis. 2015;39:9–12. doi: 10.1016/j.cimid.2015.01.002. [DOI] [PubMed] [Google Scholar]
  24. Narapakdeesakul D., Kaewparuehaschai M., Thongsahuan S., Lekcharoen P., Pengsakul T., Pattaradilokrat S., Kaewthamasorn M. Multi-locus sequence analysis of 'Candidatus Mycoplasma haematomacacae' in free-ranging macaques from Thailand suggestive of a closer relationship to hemotropic mycoplasmas in capuchins and potential origin from bats. Acta Trop. 2024;252 doi: 10.1016/j.actatropica.2024.107156. [DOI] [PubMed] [Google Scholar]
  25. Roos C., Boonratana R., Supriatna J., Fellowes J.R., Groves C.P., Nash S.D., Rylands A.B., Mittermeier R.A. An updated taxonomy and conservation status review of Asian Primates. Asian Primates J. 2014;4(1):2–38. [Google Scholar]
  26. Rucksaken R., Kaewchot S., Jarudecha T., Vitithumakhun N., Niyomdham J., Ngamkala S., Sricharern W. Molecular detection and characterization of hemotropic mycoplasma in Assamese macaques (Macaca assamensis) of Northern Thailand. Vet. Med. Int. 2024 doi: 10.1155/2024/5539938. 2024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sashida H., Suzuki Y., Rokuhara S., Nagai K., Harasawa R. Molecular demonstration of hemotropic mycoplasmas in wild Japanese monkeys (Macaca fuscata) J. Vet. Med. Sci. 2014;76(1):97–101. doi: 10.1292/jvms.13-0332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schurer J.M., Ramirez V., Kyes P., Tanee T., Patarapadungkit N., Thamsenanupap P., Trufan S., Grant E.T., Garland-Lewis G., Kelley S., Nueaitong H., Kyes R.C., Rabinowitz P. Long-Tailed macaques (Macaca fascicularis) in urban landscapes: gastrointestinal parasitism and barriers for healthy coexistence in Northeast Thailand. Am. J. Trop. Med. Hyg. 2019;100(2):357–364. doi: 10.4269/ajtmh.18-0241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sharifiyazdi H., Nazifi S., Shirzad Aski H., Shayegh H. Molecular characterization and phylogenetic analysis of the causative agent of hemoplasma infection in small Indian Mongoose (Herpestes Javanicus) Comp. Immunol. Microbiol. Infect. Dis. 2014;37(4):243–247. doi: 10.1016/j.cimid.2014.07.002. [DOI] [PubMed] [Google Scholar]
  30. Sricharern W., Kaewchot S., Kaewmongkol S., Inthong N., Jarudecha T., Rucksaken R., Mangkit B., Wichianchot S., Inpankaew T. Detection and genetic characterization of "Candidatus Mycoplasma haemomacaque" infection among long-tailed macaques (Macaca fascicularis) in Thailand using broad-range nested polymerase chain reaction assay. Vet. World. 2021;14(4):943–948. doi: 10.14202/vetworld.2021.943-948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Suksai P., Kaewchot S., Sereerak P., Boonnan S., Phimsin B., Jaruwattananon T., Raschasin K., Kaewparuehaschai M., Siriphet S., Bhusri B. Molecular identification of hemoplasmas in free ranging non–human primates in Thailand. Asian Pac. J. Tropical Med. 2019;12(8) doi: 10.4103/1995-7645.262565. [DOI] [Google Scholar]
  32. Suwannarong K., Soonthornworasiri N., Maneekan P., Balthip K., Yimsamran S., Maneewatchararangsri S., Ponlap T., Saengkul C., Lantican C., Thammasutti K., Singhasivanon P. Love or conflict: a qualitative study of the human-long tailed macaque interface in Nakhon Sawan Province, Thailand. Acta Trop. 2023;240 doi: 10.1016/j.actatropica.2023.106861. [DOI] [PubMed] [Google Scholar]
  33. Sykes J.E., Lindsay L.L., Maggi R.G., Breitschwerdt E.B. Human coinfection with Bartonella henselae and two hemotropic mycoplasma variants resembling Mycoplasma ovis. J. Clin. Microbiol. 2010;48(10):3782–3785. doi: 10.1128/JCM.01029-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Willi B., Boretti F.S., Tasker S., Meli M.L., Wengi N., Reusch C.E., Lutz H., Hofmann-Lehmann R. From Haemobartonella to hemoplasma: molecular methods provide new insights. Vet. Microbiol. 2007;125(3–4):197–209. doi: 10.1016/j.vetmic.2007.06.027. [DOI] [PubMed] [Google Scholar]
  35. Yuan C.L., Liang A.B., Yao C.B., Yang Z.B., Zhu J.G., Cui L., Yu F., Zhu N.Y., Yang X.W., Hua X.G. Prevalence of Mycoplasma suis (Eperythrozoon suis) infection in swine and swine-farm workers Shanghai, China. Am. J. Vet. Res. 2009;70(7):890–894. doi: 10.2460/ajvr.70.7.890. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The partial 16S rRNA sequences of ‘Candidatus Mycoplasma haematomacacae’ obtained in this study were deposited in the GenBank™ database (https://www.ncbi.nlm.nih.gov/nuccore) under the accession numbers PX998692–PX998766.

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