Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulation

Abstract

A collection of 259 staphylococci of 13 different species [212 coagulase-negative (CoNS) and 47 coagulase-positive (CoPS)] recovered from nasotracheal samples of 87 healthy nestling white storks was tested by the spot-on-lawn method for antimicrobial-activity (AA) against 14 indicator bacteria. Moreover, extracts of AP isolates were obtained [cell-free-supernatants (CFS) both crude and concentrated and butanol extracts] and tested against the 14 indicator bacteria. The microbiota modulation capacity of AP isolates was tested considering: (a) intra-sample AA, against all Gram-positive bacteria recovered in the same stork nasotracheal sample; (b) inter-sample AA against a selection of representative Gram-positive bacteria of the nasotracheal microbiota of all the storks (30 isolates of 29 different species and nine genera). In addition, enzymatic susceptibility test was carried out in selected AP isolates and bacteriocin encoding genes was studied by PCR/sequencing. In this respect, nine isolates (3.5%; seven CoNS and two CoPS) showed AA against at least one indicator bacteria and were considered antimicrobial-producing (AP) isolates. The AP isolates showed AA only for Gram-positive bacteria. Three of these AP isolates (S. hominis X3764, S. sciuri X4000, and S. chromogenes X4620) revealed AA on all extract conditions; other four AP isolates only showed activity in extracts after concentration; the remaining two AP isolates did not show AA in any of extract conditions. As for the microbiota modulation evaluation, three of the nine AP-isolates revealed intra-sample AA. It is to highlight the potent inter-sample AA of the X3764 isolate inhibiting 73% of the 29 representative Gram-positive species of the nasotracheal stork microbiota population. On the other hand, enzymatic analysis carried out in the two highest AP isolates (X3764 and X4000) verified the proteinaceous nature of the antimicrobial compound and PCR analysis revealed the presence of lantibiotic-like encoding genes in the nine AP isolates. In conclusion, these results show that nasotracheal staphylococci of healthy storks, and especially CoNS, produce antimicrobial substances that could be important in the modulations of their nasal microbiota.

Addressing Challenges in Wildlife Rehabilitation: Antimicrobial-Resistant Bacteria from Wounds and Fractures in Wild Birds

“…On the other hand, the absence of CHLresistant isolates found in the present study contrasts with results obtained by Sousa et al in a study of the characterization of staphylococci isolated from the nasal cavity in wild birds (71.3%) [47]. Resistance to ERY, CIP, TET, and SXT has also been observed in lower proportions in similar studies with wild birds [14,37,40,48,51].…”

“…Even though ARB should be expected to be in a lower proportion in wild birds, some species, such as white storks (Ciconia Ciconia) or Columbiformes, are considered urban birds and have closer contact with human activities and garbage, increasing the risk of acquiring ARB [25,48]. Clindamycin was the antimicrobial with the highest rate of resistance (54.5%), which agrees with previous reports from wildlife [14,19,23,37,49]. Ruiz-Ripa et al [40] detected 90% of CMN-resistant staphylococci, highlighting a potential conflict with veterinary clinical procedures as clindamycin is widely used, especially for pododermatitis and osteomyelitis treatment in wild birds [5,14].…”

“…It is one of the genera with the highest resistance to antimicrobials, which makes its treatment extremely difficult, and S. aureus is considered one of the most lethal resistant bacteria worldwide, which globally had been indirectly associated with more than 4 million deaths in 2019 [21]. In addition, due to its ubiquity and easy cultivation, it has been used in numerous studies as a sentinel bacterium to study AMR trends [36,37]. The source of these bacteria colonizing injuries from wild birds might be related to scratches or bites from other animals, especially in urban wild birds.…”

Comprehensive Approaches for the Search and Characterization of Staphylococcins

“…There is little information about the detection of staphylococcins in staphylococci of wild animals. However, in a recent study, antimicrobial substances of Staphylococcus from migratory birds were detected and their potential role in nasotracheal microbiota modulation was analyzed [ 20 ].…”

“…In recent times, increasing research focusing on the characterization, mechanisms, activity (mostly against S. aureus ), safety evaluation (including cytotoxicity), and regulations of bacteriocins detected in staphylococci have been reported [ 7 , 19 ]. Recently, we identified and characterized some relevant bacteriocin-producing staphylococci from animal, human, and environmental sources in our laboratory [ 20 , 21 , 22 ].…”