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Front. Microbiol. | doi: 10.3389/fmicb.2018.02863

Commentary: Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies

 Arinjay Banerjee1, Edel Pérez-López2 and  Karen Mossman1*
  • 1McMaster University, Canada
  • 2University of Saskatchewan, Canada

In their article, Carrillo-Araujo et al. show that Phyllostomidae (New World leaf-nosed bat family) gut microbiome composition is closely associated with host phylogeny. They provide evidence that feeding-strategy plays a role in the microbiome composition of these bats (Carrillo-Araujo et al., 2015). We were particularly intrigued by their detection of deoxyribonucleic acid (DNA) from Firmicutes in intestinal sections from these bats. Mollicutes (Phylum Firmicutes) are a class of microorganisms that include phytoplasmas (‘Candidatus Phytoplasma’) that are being increasingly recognized for their role in plant diseases such as sapodilla little leaf, yellow leaf roll disease of peach, strawberry green petal and sugarcane white leaf syndrome. These diseases affect a diverse array of economically and ecologically important plant hosts around the world (Vesterinen et al., 2013;Perez-Lopez et al., 2016;Perez-Lopez et al., 2017).

In their article, the authors indicate that Artibeus jamaicensis have the highest relative abundance of Mollicutes in their intestinal contents (Carrillo-Araujo et al., 2015). Supplementary table S1 also indicates the presence of nucleic acids from Firmicutes in all bat species that were sampled. Looking at their data from a plant disease perspective, we wondered if frugivorous and nectivorous bats could play a role in the transmission of plant pathogens. Could this data set and the sampling methods established allow us to monitor bats as sentinels of plant pathogens? Here, we speculate upon the role of frugivorous and nectivorous bats as possible vectors of plant pathogens. We outline limitations of this study that do not allow us to fully establish the dynamics of plant pathogen-bat interactions. We also discuss future directions to firmly establish the role of bats as potential vectors of plant pathogens.

Recently, bats have been implicated as the reservoirs of several emerging viruses that cause serious disease in humans and agricultural animals (Calisher et al., 2006;Moratelli and Calisher, 2015;Zhou et al., 2018). These viruses fail to cause disease symptoms in experimentally or naturally infected bats (Munster et al., 2016;Hu et al., 2017;Schuh et al., 2017). We and others have since identified several adaptations in innate immune signaling molecules that might allow bats to control virus propagation more effectively than other mammals (Zhou et al., 2016;Banerjee et al., 2017;Xie et al., 2018). Bats are also recognized as potential reservoirs of pathogenic bacteria (Loftis et al., 2005;Becker et al., 2018). Plant pathogens do not generally infect mammalian hosts, but after careful analysis of Carrillo-Araujo et al.’s article (Carrillo-Araujo et al., 2015), the role of bats as potential vectors/carriers of plant pathogens cannot be ruled out. We compared the extent of spread of phytoplasmas in the Americas (Fig 1A) and observed that it overlapped with the spread of frugivorous bats A. jamaicensis (Fig 1B) and Carollia perspicillata (Fig 1C) and nectivorous bats Leptonycteris yerbabuenae (Fig 1D) and Glossophaga soricina (Fig 1E) that were sampled by the authors. The authors mention that frugivorous and nectivorous bats diverged 20-18 million years ago (MYA). Evolutionary reconstructions show that the divergence of Mollicutes into two major branches occurred about 470 MYA, placing phytoplasmas and their closest ancestor, Acholeplasmas in the same branch (Maniloff, 2002). There is further evidence that phytoplasmas diverged from an Acholeplasma-like ancestor around 99 MYA (Zhao et al., 2015). Thus, phytoplasmas and fruigivorous bats have co-existed for at least 18 million years. Could bats have acquired phytoplasmas as part of their microbiome after their divergence into frugivorous and nectivorous bats? Could bats have played a role in phytoplasmas spread? We do not know. Phytoplasmas have been detected in fruits in the United States and Canada (Bagadia et al., 2013;Rosete et al., 2015). There is a need to sample additional bat species to fully elucidate the overlap in the spread of phytoplasmas and frugivorous bats.

Multiple studies have established the role of bats as reservoirs of certain mammalian viruses (Corman et al., 2014;Plowright et al., 2016;Ng and Tan, 2017;Noh et al., 2017;Widagdo et al., 2017). Similar studies are needed for plant pathogens. In this study, the authors analyzed the microbiome of bats using DNA sequencing. The ability to culture Mollicutes from bat intestinal samples would identify if these bacteria remain viable while they pass through the harsh environment of the digestive tract. Unfortunately, many of the plant pathogenic Mollicutes, including phytoplasmas, are unculturable in axenic media. Although Mollicutes are unlikely to replicate in bat gut cells, they could potentially proliferate within the intestinal micro-community. However, this remains to be tested.

Other questions about the possible excretion of viable bacteria through bat guano and the ability to infect plants remain unknown (Fig 1F). Seeds could be part of bat guano, but phytoplasma transmission through seeds has not been confirmed or disproved yet. Alongside birds, bats are capable of true flight. The possibility to deposit phytoplasma-contaminated guano from one area to another and within the same area is high. Aryan et al. showed that phytoplasmas are transmissible through graft (Aryan et al., 2016). Thus, mechanical transmission is another possibility. This form of transmission occurs when feeding animals cause tissue damage in plants, aiding the spread of microorganisms.

While bats are speculated as reservoirs of multiple microbes, this study brings up the possibility of using bat microbiome data as predictors of pathogen spread and prevalence (Fig 1F). Although our knowledge about the bat microbiome is limited, it does provide us with an opportunity to study bats as sentinels of plant pathogens. This opportunity extends to insect-eating bats, since insects such as leafhoppers and planthoppers are known vectors for phytoplasmas (Weintraub and Beanland, 2006;Pérez-López et al., 2018).

Future studies focused on identifying neglected vectors of plant pathogens will elucidate the likely role played by herbivorous wildlife in the dispersal of these microorganisms. Results from such studies will have agricultural policy implications for plant diseases. Phytoplasmas continue to cause losses to local farmers and has an impact on the economy. In our opinion, this study by Carrillo-Araujo et al. that identified Mollicutes in the intestinal content of Phyllostomid bats opens up an alternate and intriguing line of investigation in to wildlife vectors and sentinels of plant pathogens.

Keywords: Phytoplasma, Plant Pathogen, microbiome, BAT, host interation

Received: 15 Oct 2018; Accepted: 06 Nov 2018.

Edited by:

Boran Kartal, Max Planck Institute for Marine Microbiology (MPG), Germany

Reviewed by:

Caleb D. Phillips, Texas Tech University, United States  

Copyright: © 2018 Banerjee, Pérez-López and Mossman. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Karen Mossman, McMaster University, Hamilton, L8S 4L8, Ontario, Canada, mossk@mcmaster.ca