Growth response of Vibrio cholerae O1 and V. cholerae non O1/non O139 strains to algae extracts from stream water in far north Cameroon
-
Moussa Djaouda
,
Roméo Wakayansam Bouba
,
Pierre Nestor Nguimbous
,
Pagoui Ehbiakbo
,
Eric Moïse Bakwo Fils
,
Céline Nguefeu Nkenfou
Abstract
Background and Objectives: Vibrio cholerae O1 or non O1/non O139 is found in water ecosystems where it colonizes phytoplankton and has different lifestyle. This study aimed to investigate the impact of some algae extracts on the survival/growth of both V. cholerae strains.
Materials and Methods: Algae extracts consisting of three fractions, F1 containing chlorophyll-a, F2 containing chlorophyll-b, and F3 containing carotenoids, and raw extract (RAE) were obtained from the algal bloom collected in the Kaliao stream (Maroua, Cameroon). The survival and growth of V. cholerae O1 and V. cholerae non O1/non O139, in microcosms consisting of sterile saline with these extracts and peptone (PEP) respectively added at concentrations of 0.01, 0.05 and 0.1 mg/L, and 50/50 mixtures F1+F2, F2+F3, and F2+PEP at a concentration 0.05 mg/L, were compared during a 24h experiment.
Results: The microcosms F2 and RAE did not support the growth of O1 strain; V. cholerae non O1/non O139 count in all algae extract microcosms ranging from 3.97 log (CFU/mL) to 5.2 log (CFU/mL). In all PEP microcosms, the counts of both strains reached an uncountable value. Microcosms F1+F2 and F2+F3 supported the growth of V. cholerae O1 and V. cholerae non-O1/nonO139 strains.
Conclusion: The algae compounds showed strain-specific effect on the growth of V. cholerae.
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5. Bueno E, Pinedo V, Cava F. Adaptation of Vibrio cholerae to hypoxic environments. Front Microbiol 2020; 11: 739.
6. Brumfield KD, Usmani M, Chen KM, Gangwar M, Jutla AS, Huq A, et al. Environmental parameters associated with incidence and transmission of pathogenic Vibrio spp. Environ Microbiol 2021; 23: 7314-7340.
7. Islam MT, Alam M, Boucher Y. Emergence, ecology and dispersal of the pandemic generating Vibrio cholerae lineage. Int Microbiol 2017; 20: 106-115.
8. Reethy PS, Lalitha KV. Characterization of V. cholerae O1 biotype El Tor serotype Ogawa possessing the ctxB gene of the classical biotype isolated from well water associated with the cholera outbreak in Kerala, South India. J Water Health 2021; 19: 478-487.
9. Shackleton D, Memon FA, Nichols G, Phalkey R, Chen AS. Mechanisms of cholera transmission via environment in India and Bangladesh: state of the science review. Rev Environ Health 2023; 39: 313-329.
10. Caroppo C, Azzaro F, Bergamasco A, Caruso G, Decembrini F. Phytoplankton and bacterial communities’ patterns in a highly dynamic ecosystem (Central Mediterranean Sea). Water 2022; 14: 2057.
11. Padovan A, Siboni N, Kaestli M, King W, Seymour J, Gibb K. Occurrence and dynamics of potentially pathogenic vibrios in the wet-dry tropics of northern Australia. Mar Environ Res 2021; 169: 105405.
12. Hoque MM, Noorian P, Espinoza-Vergara G, Manuneedhi Cholan P, Kim M, Rahman MH, et al. Adaptation to an amoeba host drives selection of virulence-associated traits in Vibrio cholerae. ISME J 2022; 16: 856-867.
13. Faruque SM, Naser IB, Islam MJ, Faruque AS, Ghosh AN, Nair GB, et al. Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc Natl Acad Sci U S A 2005; 102: 1702-1707.
14. Islam MS, Zaman MH, Islam MS, Ahmed N, Clemens JD. Environmental reservoirs of Vibrio cholerae. Vaccine 2020; 38 Suppl 1: A52-A62.
15. Islam MS, Islam MS, Mahmud ZH, Cairncross S, Clemens JD, Collins AE. Role of phytoplankton in maintaining endemicity and seasonality of cholera in Bangladesh. Trans R Soc Trop Med Hyg 2015; 109: 572-578.
16. Islam MS, Mahmuda S, Morshed MG, Bakht HB, Khan MN, Sack RB, et al. Role of cyanobacteria in the persistence of Vibrio cholerae O139 in saline microcosms. Can J Microbiol 2004; 50: 127-131.
17. Osborne B, Siboni N, Seymour JR, Ralph P, Pernice M. Exploring the potential of algae‑bacteria interactions in the biocontrol of the marine pathogen Vibrio parahaemolyticus. J Appl Phycol 2023; 35: 2731-2743.
18. Hamad GM, Samy H, Mehany T, Korma SA, Eskander M, Tawfik RG, et al. Utilization of algae extracts as natural antibacterial and antioxidants for controlling foodborne bacteria in meat products. Foods 2023; 12: 3281.
19. Anas A, Krishna K, Vijayakumar S, George G, Menon N, Kulk G, et al. Dynamics of Vibrio cholerae in a typical tropical lake and estuarine system: potential of remote sensing for risk mapping. Remote Sens 2021; 13: 1034.
20. Ouamba JP, Mbarga NF, Ciglenecki I, Ratnayake R, Tchiasso D, Finger F, et al. Implementation of targeted cholera response activities, Cameroon. Bull World Health Organ 2023; 101: 170-178.
21. El-Sapagh S, El-Shenody R, Pereira L, Elshobary M. Unveiling the potential of algal extracts as promising antibacterial and antibiofilm agents against multidrug-resistant Pseudomonas aeruginosa: in vitro and in silico studies including molecular docking. Plants (Basel) 2023; 12: 3324.
22. Yanda L, Tatsimo SJN, Tamokou JD, Matsuete-Takongmo G, Meffo-Dongmo SC, Meli Lannang A, et al. Antibacterial and antioxidant activities of isolated compounds from Prosopis Africana Leaves. Int J Anal Chem 2022; 2022: 4205823.
23. Susanti I, Pratiwi R, Rosanti Y, Hasanah AN. Separation methods of phenolic compounds from plant extract as antioxydant agents candidate. Plants (Basel) 2024; 13: 965.
24. Global Task Force on Cholera Control. Public health surveillance for cholera. Guidance document (2024). https://www.gtfcc.org/wp-content/uploads/2024/04/public-health-surveillance-for-cholera-guidance-document-2024.pdf
25. Djaouda M, Wadoubé Z, Baponwa O, Youssoufa S, Gaké B, Liang S, et al. Survival and growth of Vibrio cholerae and Escherichia coli in treated groundwater consumed in northern Cameroon. Appl Water Sci 2020; 10: 242.
26. Fang T, Zhang Z, Wang H, Rogers M, Cui Q. Insights into effects of algae on decay and distribution of bacterial pathogens in recreational water: implications for microbial risk management. J Environ Sci (China) 2022; 113: 92-103.
27. Basu S, Pal A, Desai PK. Quality control of culture media in a microbiology laboratory. Indian J Med Microbiol 2005; 23: 159-163.
28. Oruganti RK, Katam K, Show PL, Gadhamshetty V, Upadhyayula VKK, Bhattacharyya D. A comprehensive review on the use of algal-bacterial systems for wastewater treatment with emphasis on nutrient and micropollutant removal. Bioengineered 2022; 13: 10412-10453.
29. Cai T, Zhang X, Zhang S, Ming Y, Zhang Q. Photochemical behaviors of dissolved organic matter in aquatic environment: generation, characterization, influencing factors and pratical application. Environ Res 2023; 231: 116174.
30. Monjerezi M, Ngongondo C. Quality of groundwater resources in Chikhwawa, Lower shire valley, Malawi. Water Qual Expo Health 2012; 4: 39-53.
31. Gomes L, Monteiro P, Cotas J, Gonçalves AMM, Fernandes C, Gonçalves T, et al. Seaweeds pigments and phenolic compounds with antimicrobial potential. Biomol Concepts 2022; 13: 89-102.
32. Hu X, Page MT, Sumida A, Tanaka A, Terry MJ, Tanaka R. The iron–sulfur cluster biosynthesis protein SUFB is required for chlorophyll synthesis, but not phytochrome signaling. Plant J 2017; 89: 1184-1194.
33. Duhutrel P, Bordat C, Wu T-D, Zagorec M, Guerquin-Kern J-L, Champomier-Vergès M-C. Iron sources used by the nonpathogenic lactic acid bacterium Lactobacillus seki as revealed by electron energy loss spectroscopy and secondary-ion mass spectrometry. Appl Environ Microbiol 2010; 76: 560-565.
34. Escobara LE, Ryana SJ, Stewart-Ibarraa AM, Finkelsteing JL, King CA, Qiaoj H, et al. A global map of suitability for coastal Vibrio cholerae under current and future climate conditions. Acta Trop 2015; 149: 202-211.
35. Schober L, Dobiašová H, Jurkaš V, Parmeggiani F, Rudroff F, Winkler M. Enzymatic reactions towards aldehydes: an overview. Flavour Fragr J 2023; 38: 221-242.
36. Naser IB, Shishir TA, Faruque SN, Hoque MM, Hasan A, Faruque SM. Environmental prevalence of toxigenic Vibrio cholerae O1 in Bangladesh coincides with V. cholerae non-O1 non-O139 genetic variants which overproduce autoinducer-2. PLoS One 2021; 16: e0254068.
37. Bhuyar P, Rahim MHA, Maniam GP, Ramaraj R, Govindan N. Exploration of bioactive compounds and antibacterial activity of marine blue-green microalgae (Oscillatoria sp.) isolated from coastal region of west Malaysia. SN Appl Sci 2020; 2: 1906.
38. Vahdati NS, Behboudi H, Tavakoli S, Aminian F, Ranjbar R. Antimicrobial potential of the green microalgae isolated from the Persian Gulf. Iran J Public Health 2022; 51: 1134-1142.
39. Cho KH, Wolny J, Kase JA, Unmo T, Pachepsky. Interaction of E. coli with algae and aquatic vegetation in natural waters. Water Res 2022; 209: 117952.
40. Naisi S, Bayat M, Zahraei Salehi T, Rahimian Zarif B, Yahyaraeyat R. Antimicrobial and anti-biofilm effects of carotenoid pigment extracted from Rhodotorula glutinis strain on food-borne bacteria. Iran J Microbiol 2023; 15: 79-88.
2. Ismail EM, Kadry M, Elshafiee EA, Ragab E, Morsy EA, Rizk O, et al. Ecoepidemiology and potential transmission of Vibrio cholerae among different environmental niches: an upcoming threat in Egypt. Pathogens 2021; 10: 190.
3. Bénard AHM, Guenou E, Fookes M, Ateudjieu J, Kasambara W, Siever M, et al. Whole genome sequence of Vibrio cholerae directly from dried spotted filter paper. PLoS Negl Trop Dis 2019; 13(5): e0007330.
4. Kaas RS, Ngandjio A, Nzouankeu A, Siriphap A, Fonkoua MC, Aarestrup F, et al. The Lake Chad basin, an isolated and persistent reservoir of Vibrio cholerae O1: a genomic insight into the outbreak in Cameroon, 2010. PLoS One 2016; 11(5): e0155691.
5. Bueno E, Pinedo V, Cava F. Adaptation of Vibrio cholerae to hypoxic environments. Front Microbiol 2020; 11: 739.
6. Brumfield KD, Usmani M, Chen KM, Gangwar M, Jutla AS, Huq A, et al. Environmental parameters associated with incidence and transmission of pathogenic Vibrio spp. Environ Microbiol 2021; 23: 7314-7340.
7. Islam MT, Alam M, Boucher Y. Emergence, ecology and dispersal of the pandemic generating Vibrio cholerae lineage. Int Microbiol 2017; 20: 106-115.
8. Reethy PS, Lalitha KV. Characterization of V. cholerae O1 biotype El Tor serotype Ogawa possessing the ctxB gene of the classical biotype isolated from well water associated with the cholera outbreak in Kerala, South India. J Water Health 2021; 19: 478-487.
9. Shackleton D, Memon FA, Nichols G, Phalkey R, Chen AS. Mechanisms of cholera transmission via environment in India and Bangladesh: state of the science review. Rev Environ Health 2023; 39: 313-329.
10. Caroppo C, Azzaro F, Bergamasco A, Caruso G, Decembrini F. Phytoplankton and bacterial communities’ patterns in a highly dynamic ecosystem (Central Mediterranean Sea). Water 2022; 14: 2057.
11. Padovan A, Siboni N, Kaestli M, King W, Seymour J, Gibb K. Occurrence and dynamics of potentially pathogenic vibrios in the wet-dry tropics of northern Australia. Mar Environ Res 2021; 169: 105405.
12. Hoque MM, Noorian P, Espinoza-Vergara G, Manuneedhi Cholan P, Kim M, Rahman MH, et al. Adaptation to an amoeba host drives selection of virulence-associated traits in Vibrio cholerae. ISME J 2022; 16: 856-867.
13. Faruque SM, Naser IB, Islam MJ, Faruque AS, Ghosh AN, Nair GB, et al. Seasonal epidemics of cholera inversely correlate with the prevalence of environmental cholera phages. Proc Natl Acad Sci U S A 2005; 102: 1702-1707.
14. Islam MS, Zaman MH, Islam MS, Ahmed N, Clemens JD. Environmental reservoirs of Vibrio cholerae. Vaccine 2020; 38 Suppl 1: A52-A62.
15. Islam MS, Islam MS, Mahmud ZH, Cairncross S, Clemens JD, Collins AE. Role of phytoplankton in maintaining endemicity and seasonality of cholera in Bangladesh. Trans R Soc Trop Med Hyg 2015; 109: 572-578.
16. Islam MS, Mahmuda S, Morshed MG, Bakht HB, Khan MN, Sack RB, et al. Role of cyanobacteria in the persistence of Vibrio cholerae O139 in saline microcosms. Can J Microbiol 2004; 50: 127-131.
17. Osborne B, Siboni N, Seymour JR, Ralph P, Pernice M. Exploring the potential of algae‑bacteria interactions in the biocontrol of the marine pathogen Vibrio parahaemolyticus. J Appl Phycol 2023; 35: 2731-2743.
18. Hamad GM, Samy H, Mehany T, Korma SA, Eskander M, Tawfik RG, et al. Utilization of algae extracts as natural antibacterial and antioxidants for controlling foodborne bacteria in meat products. Foods 2023; 12: 3281.
19. Anas A, Krishna K, Vijayakumar S, George G, Menon N, Kulk G, et al. Dynamics of Vibrio cholerae in a typical tropical lake and estuarine system: potential of remote sensing for risk mapping. Remote Sens 2021; 13: 1034.
20. Ouamba JP, Mbarga NF, Ciglenecki I, Ratnayake R, Tchiasso D, Finger F, et al. Implementation of targeted cholera response activities, Cameroon. Bull World Health Organ 2023; 101: 170-178.
21. El-Sapagh S, El-Shenody R, Pereira L, Elshobary M. Unveiling the potential of algal extracts as promising antibacterial and antibiofilm agents against multidrug-resistant Pseudomonas aeruginosa: in vitro and in silico studies including molecular docking. Plants (Basel) 2023; 12: 3324.
22. Yanda L, Tatsimo SJN, Tamokou JD, Matsuete-Takongmo G, Meffo-Dongmo SC, Meli Lannang A, et al. Antibacterial and antioxidant activities of isolated compounds from Prosopis Africana Leaves. Int J Anal Chem 2022; 2022: 4205823.
23. Susanti I, Pratiwi R, Rosanti Y, Hasanah AN. Separation methods of phenolic compounds from plant extract as antioxydant agents candidate. Plants (Basel) 2024; 13: 965.
24. Global Task Force on Cholera Control. Public health surveillance for cholera. Guidance document (2024). https://www.gtfcc.org/wp-content/uploads/2024/04/public-health-surveillance-for-cholera-guidance-document-2024.pdf
25. Djaouda M, Wadoubé Z, Baponwa O, Youssoufa S, Gaké B, Liang S, et al. Survival and growth of Vibrio cholerae and Escherichia coli in treated groundwater consumed in northern Cameroon. Appl Water Sci 2020; 10: 242.
26. Fang T, Zhang Z, Wang H, Rogers M, Cui Q. Insights into effects of algae on decay and distribution of bacterial pathogens in recreational water: implications for microbial risk management. J Environ Sci (China) 2022; 113: 92-103.
27. Basu S, Pal A, Desai PK. Quality control of culture media in a microbiology laboratory. Indian J Med Microbiol 2005; 23: 159-163.
28. Oruganti RK, Katam K, Show PL, Gadhamshetty V, Upadhyayula VKK, Bhattacharyya D. A comprehensive review on the use of algal-bacterial systems for wastewater treatment with emphasis on nutrient and micropollutant removal. Bioengineered 2022; 13: 10412-10453.
29. Cai T, Zhang X, Zhang S, Ming Y, Zhang Q. Photochemical behaviors of dissolved organic matter in aquatic environment: generation, characterization, influencing factors and pratical application. Environ Res 2023; 231: 116174.
30. Monjerezi M, Ngongondo C. Quality of groundwater resources in Chikhwawa, Lower shire valley, Malawi. Water Qual Expo Health 2012; 4: 39-53.
31. Gomes L, Monteiro P, Cotas J, Gonçalves AMM, Fernandes C, Gonçalves T, et al. Seaweeds pigments and phenolic compounds with antimicrobial potential. Biomol Concepts 2022; 13: 89-102.
32. Hu X, Page MT, Sumida A, Tanaka A, Terry MJ, Tanaka R. The iron–sulfur cluster biosynthesis protein SUFB is required for chlorophyll synthesis, but not phytochrome signaling. Plant J 2017; 89: 1184-1194.
33. Duhutrel P, Bordat C, Wu T-D, Zagorec M, Guerquin-Kern J-L, Champomier-Vergès M-C. Iron sources used by the nonpathogenic lactic acid bacterium Lactobacillus seki as revealed by electron energy loss spectroscopy and secondary-ion mass spectrometry. Appl Environ Microbiol 2010; 76: 560-565.
34. Escobara LE, Ryana SJ, Stewart-Ibarraa AM, Finkelsteing JL, King CA, Qiaoj H, et al. A global map of suitability for coastal Vibrio cholerae under current and future climate conditions. Acta Trop 2015; 149: 202-211.
35. Schober L, Dobiašová H, Jurkaš V, Parmeggiani F, Rudroff F, Winkler M. Enzymatic reactions towards aldehydes: an overview. Flavour Fragr J 2023; 38: 221-242.
36. Naser IB, Shishir TA, Faruque SN, Hoque MM, Hasan A, Faruque SM. Environmental prevalence of toxigenic Vibrio cholerae O1 in Bangladesh coincides with V. cholerae non-O1 non-O139 genetic variants which overproduce autoinducer-2. PLoS One 2021; 16: e0254068.
37. Bhuyar P, Rahim MHA, Maniam GP, Ramaraj R, Govindan N. Exploration of bioactive compounds and antibacterial activity of marine blue-green microalgae (Oscillatoria sp.) isolated from coastal region of west Malaysia. SN Appl Sci 2020; 2: 1906.
38. Vahdati NS, Behboudi H, Tavakoli S, Aminian F, Ranjbar R. Antimicrobial potential of the green microalgae isolated from the Persian Gulf. Iran J Public Health 2022; 51: 1134-1142.
39. Cho KH, Wolny J, Kase JA, Unmo T, Pachepsky. Interaction of E. coli with algae and aquatic vegetation in natural waters. Water Res 2022; 209: 117952.
40. Naisi S, Bayat M, Zahraei Salehi T, Rahimian Zarif B, Yahyaraeyat R. Antimicrobial and anti-biofilm effects of carotenoid pigment extracted from Rhodotorula glutinis strain on food-borne bacteria. Iran J Microbiol 2023; 15: 79-88.
| Files | ||
| Issue | Vol 16 No 5 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i5.16796 | |
| Keywords | ||
| Vibrio cholerae; Algae; Survival; Water; Chlorophyll; Carotenoids | ||
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How to Cite
1.
Djaouda M, Wakayansam Bouba R, Nguimbous PN, Ehbiakbo P, Bakwo Fils EM, Nguefeu Nkenfou C. Growth response of Vibrio cholerae O1 and V. cholerae non O1/non O139 strains to algae extracts from stream water in far north Cameroon. Iran J Microbiol. 2024;16(5):631-638.
