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Alien vs. Predator: Pathogens open niche space for opportunists

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  • A peer-reviewed version of this preprint was published in PeerJ on 31May 2017.

    View the peer-reviewed version (peerj.com/articles/3315), which is thepreferred citable publication unless you specifically need to cite this preprint.

    Welsh RM, Rosales SM, Zaneveld JR, Payet JP, McMinds R, Hubbs SL, VegaThurber RL. (2017) Alien vs. predator: bacterial challenge alters coralmicrobiomes unless controlled by Halobacteriovorax predators. PeerJ 5:e3315https://doi.org/10.7717/peerj.3315

    https://doi.org/10.7717/peerj.3315https://doi.org/10.7717/peerj.3315

  • Alien vs. Predator: Pathogens open niche space foropportunists, unless controlled by predatorsRory M Welsh, Rebecca Vega Thurber, Jesse R.R. Zaneveld, Jerome P Payet, Ryan McMinds, Stephanie M Rosales, Steve L Hubbs

    Coral microbiomes are known to play important roles in organismal health, response toenvironmental stress, and resistance to disease. Pathogens invading the coral microbiomeencounter diverse assemblages of resident bacteria, ranging from defensive and metabolicsymbionts to opportunistic bacteria that may turn harmful in compromised hosts.However, little is known about how these bacterial interactions influence the overallstructure, stability, and function of the microbiome during the course of pathogenchallenge. We sought to test how coral microbiome dynamics were affected byinteractions between two of its members: Vibrio coralliilyticus, a known temperature-dependent coral pathogen, and Halobacteriovorax, a unique bacterial predator of Vibrioand other gram-negative bacteria. We challenged specimens of the important reef-buildingcoral Montastraea cavernosa with Vibrio coralliilyticus pathogens in the presence orabsence of Halobacteriovorax predators, and monitored microbial community dynamicswith 16S rRNA gene time-series. In addition to its direct effects on corals, pathogenchallenge reshaped coral microbiomes in ways that allowed for secondary blooms ofopportunistic bacteria. As expected, Vibrio coralliilyticus addition increased the infiltrationof Vibrio into coral tissues. This increase of Vibrios in coral tissue was accompanied byincreased richness, and reduced stability (increased beta-diversity) of the rest of themicrobiome, suggesting strong secondary effects of pathogen invasion on commensal andmutualistic coral bacteria. Moreover, after an initial increase in Vibrios, two opportunisticlineages (Rhodobacterales and Cytophagales) increased in coral tissues, suggesting thatthis pathogen opens niche space for opportunists. Based on the keystone role of predatorsin many ecosystems, we hypothesized that Halobacteriovorax predators might helpprotect corals by consuming gram-negative pathogens. In keeping with a protective role,Halobacteriovorax addition alone had only minor effects on the microbiome, and noinfiltration of Halobacteriovorax into coral tissues was detected in amplicon libraries.Simultaneous challenge with both pathogen and predator eliminated detectable V.corallyticus infiltration into coral tissue samples, ameliorated changes to the rest of thecoral microbiome, and prevented secondary blooms of opportunistic Rhodobacterales andCytophagales. Thus, we show that primary infection by a coral pathogen is sufficient to

    PeerJ PrePrints | https://dx.doi.org/10.7287/peerj.preprints.1537v1 | CC-BY 4.0 Open Access | rec: 26 Nov 2015, publ: 26 Nov 2015

  • cause increases in opportunists, as seen in correlational studies. These data furtherprovide a proof-of-principle demonstration that, under certain circumstances, host-associated bacterial predators can mitigate the ability of pathogens to infiltrate hosttissue, and stabilize the microbiome against complex secondary changes that favor growthof opportunistic lineages.

    PeerJ PrePrints | https://dx.doi.org/10.7287/peerj.preprints.1537v1 | CC-BY 4.0 Open Access | rec: 26 Nov 2015, publ: 26 Nov 2015

  • 1 Alien vs. Predator: Pathogens open niche space for opportunists, unless controlled by

    2 predators

    3

    4 Rory M. Welsh1, Stephanie M. Rosales1, Jesse R. Zaneveld1, Jrme P. Payet1, Ryan McMinds1,

    5 Steven L. Hubbs1, and Rebecca Vega Thurber1

    6 1Oregon State University, Dept. of Microbiology, 454 Nash Hall, Corvallis, OR, 97331, USA

    7

    8 Corresponding Author:

    9 Rebecca Vega Thurber1

    10 Oregon State University, Dept. of Microbiology, 454 Nash Hall, Corvallis, OR, 97331, USA

    11 Email address: [email protected]

    12

    PeerJ PrePrints | https://dx.doi.org/10.7287/peerj.preprints.1537v1 | CC-BY 4.0 Open Access | rec: 26 Nov 2015, publ: 26 Nov 2015

  • 13 Abstract:

    14 Coral microbiomes are known to play important roles in organismal health, response to

    15 environmental stress, and resistance to disease. Pathogens invading the coral microbiome

    16 encounter diverse assemblages of resident bacteria, ranging from defensive and metabolic

    17 symbionts to opportunistic bacteria that may turn harmful in compromised hosts. However, little

    18 is known about how these bacterial interactions influence the overall structure, stability, and

    19 function of the microbiome during the course of pathogen challenge. We sought to test how coral

    20 microbiome dynamics were affected by interactions between two of its members: Vibrio

    21 coralliilyticus, a known temperature-dependent coral pathogen, and Halobacteriovorax, a unique

    22 bacterial predator of Vibrio and other gram-negative bacteria. We challenged specimens of the

    23 important reef-building coral Montastraea cavernosa with Vibrio coralliilyticus pathogens in the

    24 presence or absence of Halobacteriovorax predators, and monitored microbial community

    25 dynamics with 16S rRNA gene time-series. In addition to its direct effects on corals, pathogen

    26 challenge reshaped coral microbiomes in ways that allowed for secondary blooms of

    27 opportunistic bacteria. As expected, Vibrio coralliilyticus addition increased the infiltration of

    28 Vibrio into coral tissues. This increase of Vibrios in coral tissue was accompanied by increased

    29 richness, and reduced stability (increased beta-diversity) of the rest of the microbiome,

    30 suggesting strong secondary effects of pathogen invasion on commensal and mutualistic coral

    31 bacteria. Moreover, after an initial increase in Vibrios, two opportunistic lineages

    32 (Rhodobacterales and Cytophagales) increased in coral tissues, suggesting that this pathogen

    33 opens niche space for opportunists. Halobacteriovorax predators are commonly present at low-

    34 abundance on coral surfaces. Based on the keystone role of predators in many ecosystems, we

    35 hypothesized that Halobacteriovorax predators might help protect corals by consuming gram-

    PeerJ PrePrints | https://dx.doi.org/10.7287/peerj.preprints.1537v1 | CC-BY 4.0 Open Access | rec: 26 Nov 2015, publ: 26 Nov 2015

  • 36 negative pathogens. In keeping with a protective role, Halobacteriovorax addition alone had only

    37 minor effects on the microbiome, and no infiltration of Halobacteriovorax into coral tissues was

    38 detected in amplicon libraries. Simultaneous challenge with both pathogen and predator

    39 eliminated detectable V. corallyticus infiltration into coral tissue samples, ameliorated changes to

    40 the rest of the coral microbiome, and prevented secondary blooms of opportunistic

    41 Rhodobacterales and Cytophagales. Thus, we show that primary infection by a coral pathogen is

    42 sufficient to cause increases in opportunists, as seen in correlational studies. These data further

    43 provide a proof-of-principle demonstration that, under certain circumstances, host-associated

    44 bacterial predators can mitigate the ability of pathogens to infiltrate host tissue, and stabilize the

    45 microbiome against complex secondary changes that favor growth of opportunistic lineages.

    46

    PeerJ PrePrints | https://dx.doi.org/10.7287/peerj.preprints.1537v1 | CC-BY 4.0 Open Access | rec: 26 Nov 2015, publ: 26 Nov 2015

  • 47

    48 Introduction

    49 Coral reefs have experienced sharp declines in coral cover from environmental factors

    50 (Death et al., 2012), temperature induced bleaching (Fitt & Warner, 1995), and disease (Bourne

    51 et al., 2009; Burge et al., 2014) with some areas of the Caribbean experiencing as much as 80%

    52 coral loss over the past several decades (Gardner et al., 2003). While many studies have

    53 identified microbial consortia that increase in diseased corals (e.g. Gignoux-Wolfsohn et al.

    54 2015), etiological agents are unknown for the majority of coral diseases (Mouchka, Hewson &

    55 Harvell, 2010). Currently Vibrio coralliilyticus is the most well described model for interactions

    56 between corals, the environment, and pathogenic bacteria (Ben-Haim et al., 2003). Several V.

    57 coralliilyticus virulence factors are temperature-dependent and upregulated above 27 C (Kimes

    58 et al., 2012), and it has been suggested that host tissue invasion can only occur above this

    59 threshold (Vidal-Dupiol et al., 2011). Given the continuous rise in sea surface temperatures due

    60 to global climate change (Hoegh-guldberg et al., 2007), and the projected increased variability of

    61 temperature extremes, it is likely that the incidence of infections by V. coralliilyticus and other

    62 temperature-dependent pathogens will increase (Maynard et al., 2015). Bacterial communities of

    63 diseased corals are also known to have large numbers of opportunistic pathogens and secondary

    64 colonizers (Gignoux-Wolfsohn & Vollmer, 2015). It has been hypothesized that the majori

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