Identification of Tenrec ecaudatus, a Wild Mammal Introduced to Mayotte Island, as a Reservoir of the Newly Identified Human Pathogenic Leptospira mayottensis

Abstract

Leptospirosis is a bacterial zoonosis of major concern on tropical islands. Human populations on western Indian Ocean islands are strongly affected by the disease although each archipelago shows contrasting epidemiology. For instance, Mayotte, part of the Comoros Archipelago, differs from the other neighbouring islands by a high diversity of Leptospira species infecting humans that includes Leptospira mayottensis, a species thought to be unique to this island. Using bacterial culture, molecular detection and typing, the present study explored the wild and domestic local mammalian fauna for renal carriage of leptospires and addressed the genetic relationships of the infecting strains with local isolates obtained from acute human cases and with Leptospira strains hosted by mammal species endemic to nearby Madagascar. Tenrec (Tenrec ecaudatus, Family Tenrecidae), a terrestrial mammal introduced from Madagascar, is identified as a reservoir of L. mayottensis. All isolated L. mayottensis sequence types form a monophyletic clade that includes Leptospira strains infecting humans and tenrecs on Mayotte, as well as two other Malagasy endemic tenrecid species of the genus Microgale. The lower diversity of L. mayottensis in tenrecs from Mayotte, compared to that occurring in Madagascar, suggests that L. mayottensis has indeed a Malagasy origin. This study also showed that introduced rats (Rattus rattus) and dogs are probably the main reservoirs of Leptospira borgpetersenii and Leptospira kirschneri, both bacteria being prevalent in local clinical cases. Data emphasize the epidemiological link between the two neighbouring islands and the role of introduced small mammals in shaping the local epidemiology of leptospirosis.

Fig 1. Bayesian phylogenetic tree of pathogenic Leptospira species from Mayotte (blue) and Madagascar (green) based on concatenated sequences of five genes (secY, adk, lipL32, lipL41 and rrs2, total size: 2215 bp).

The analysis was realized under the GTR+G substitution model. At the nodes, grey and white circles indicate posterior probabilities superior to 0.70 and 0.90, respectively. Strain numbers of cultures produced herein are indicated in parentheses, “K” and “U” designating the sequences obtained from kidney or urine, respectively. Stars indicate lineages common to humans and animals (Rattus rattus or Tenrec ecaudatus). For Homo sapiens str. 200901122, the same sequence type was found in nine cultures from T. ecaudatus (2014TE MDI222, 2014TE MDI224, 2014TE MDI294U, 2014TE MDI295, 2014TE MDI295U, 2014TE MDI306, 2014TE MD308, 2014TE MDI321 and 2014TE MDI321U). For H. sapiens str. 200701204, 200900806, 200901483 and 201003760, the same sequence type found was in seven cultures from R. rattus (2014RR MDI247, 2014RR MDI250, 2014RR MDI251, 2014RR MDI259, 2014RR MDI260, 2014RR MDI284 and 2014RR MDI291). Specimen system: MDI = CRVOI specimen catalogue during field trips to Mayotte; FMNH = Field Museum of Natural History, Chicago; UADBA = Université d’Antananarivo, Département de Biologie Animale, Madagascar; for the other bacterial sequences from H. sapiens and Microgale spp. see Bourhy et al. 2012 [15] and Dietrich et al. 2014 [4]. Museum numbers for Microgale spp.: 575 = UADBA 30869; 588 = UADBA 30289; 590 = UADBA 30291; 1335 = UADBA 32122; 1453 = UADBA 32125; 1467 = UADBA 32101.