A community perspective on the concept of marine holobionts: state-of-the-art, challenges, and future directions

Alexey Vorobev (CEA); Arite Bigalke; Ashwin Engelen (CCMAR); Catherine Leblanc (LBI2M); Claire Gachon; Damien Eveillard (LS2N); Derek Skillings; Ehsan Kayal (FR2424); Elena Kazamia (IBENS); Enora Briand (IFREMER Nantes)

arxiv: 1907.05017 · v1 · pith:OC63G2BTnew · submitted 2019-07-11 · 🧬 q-bio.PE

A community perspective on the concept of marine holobionts: state-of-the-art, challenges, and future directions

Simon Dittami (LBI2M) , Enrique Arboleda (SBR) , Jean-Christophe Auguet (UMR MARBEC) , Arite Bigalke , Enora Briand (IFREMER Nantes) , Paco C\'ardenas , Ulisse Cardini , Johan Decelle

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Ashwin Engelen (CCMAR) Damien Eveillard (LS2N) Claire Gachon Sarah Griffiths Tilmann Harder Ehsan Kayal (FR2424) Elena Kazamia (IBENS) Fran\c{c}ois Lallier (ABICE) M\'onica Medina (PSU) Ezequiel Marzinelli (SCELSE USIMS) Teresa Morganti Laura Pons Soizic Prado (MCAM) Jos\'e Pintado Valverde Mahasweta Saha Marc-Andre Selosse (OSEB) Derek Skillings Willem Stock Shinichi Sunagawa Eve Toulza (IHPE) Alexey Vorobev (CEA) Catherine Leblanc (LBI2M) Fabrice Not

This is my paper

Pith reviewed 2026-05-24 22:52 UTC · model grok-4.3

classification 🧬 q-bio.PE

keywords holobiontmarineconceptevolutionarysystemstogetherwillbiological

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The pith

The holobiont concept treats a host and its microbiota as a single coherent unit whose joint study is required to understand marine biology, ecology, and evolution, while highlighting challenges that must be addressed through community efforts.

A machine-rendered reading of the paper's core claim, the machinery that carries it, and where it could break.

Marine ecosystems depend on interactions between larger organisms and the microbes living with them. These relationships are important but poorly understood in terms of how they work, how they evolved, and what they mean for the environment. The holobiont idea treats the host and its microbes as one long-term unit that should be studied together rather than in isolation. This view aims to improve understanding of how these systems function as a whole. The paper reviews current knowledge, points out opportunities, and lists major challenges such as connecting detailed studies of simple systems with large-scale observations. It notes possible effects on economics, society, and the environment, drawing comparisons to land-based research. Progress will need better tools and closer collaboration among scientists to answer questions about ecology, evolution, and the role of these units in ocean chemistry cycles.

Core claim

The holobiont concept posits that a host and its associated microbiota, living together in a long-lasting relationship, form the holobiont, and have to be studied together, as a coherent biological and functional unit, in order to understand the biology, ecology and evolution of the organisms.

Load-bearing premise

That hosts and their microbiota form long-lasting relationships that constitute coherent functional units whose study as integrated wholes is necessary to advance understanding, as opposed to studying components independently.

read the original abstract

Host-microbe interactions play crucial roles in marine ecosystems, but we still have very little understanding of the mechanisms that govern these relationships, the evolutionary processes that shape them, and their ecological consequences. The holobiont concept is a renewed paradigm in biology that can help describe and understand these complex systems. It posits that a host and its associated microbiota, living together in a long-lasting relationship, form the holobiont, and have to be studied together, as a coherent biological and functional unit, in order to understand the biology, ecology and evolution of the organisms. Here we discuss critical concepts and opportunities in marine holobiont research and identify key challenges in the field. We highlight the potential economic, sociological, and environmental impacts of the holobiont concept in marine biological, evolutionary, and environmental sciences with comparisons to terrestrial science whenever appropriate. A deeper understanding of such complex systems, however, will require further technological and conceptual advances. The most significant challenge will be to bridge functional research on simple and tractable model systems and global approaches. This will require scientists to work together as an (inter)active community in order to address, for instance, ecological and evolutionary questions and the roles of holobionts in biogeochemical cycles.

Editorial analysis

A structured set of objections, weighed in public.

Desk editor's note, referee report, simulated authors' rebuttal, and a circularity audit. Tearing a paper down is the easy half of reading it; the pith above is the substance, this is the friction.

Desk Editor's Note private letter to a colleague

This is a community perspective that restates the holobiont framing for marine systems and lists open challenges without new data or tests.

read the letter

This paper gathers a large group of marine researchers to restate the holobiont idea—that hosts and their microbes form long-lasting functional units that should be studied together—and to flag practical challenges ahead. It adds no new measurements, models, or derivations beyond what is already in the cited literature on host-microbe interactions. The text is explicitly a discussion piece rather than a research report. What it does reasonably well is collect community input on specific bottlenecks, such as moving from tractable lab models to field-scale biogeochemical questions, and it notes potential downstream effects on applied marine science. The side-by-side notes on terrestrial holobiont work give a quick orientation for readers who work across systems. The central assumption that integrated study is necessary rather than optional is presented as a starting point, not as a claim backed by comparative evidence here. That is a limitation of the format, not a hidden flaw; the paper does not pretend to test it. No circular definitions or unfalsifiable predictions appear. The writing stays within the bounds of a perspective and avoids overclaiming. Readers already active in marine microbiology or symbiosis ecology will find the compiled list of challenges and the call for coordinated work useful as a reference point. Outsiders looking for fresh mechanistic insight or quantitative advances will not. A journal that publishes perspectives should send this to review; the community authorship and the concrete open questions make it worth referee time even though the core framing is not original.

Referee Report

0 major / 2 minor

Summary. The manuscript is a community perspective paper that defines the holobiont as a host and its associated microbiota living in a long-lasting relationship that forms a coherent biological and functional unit requiring integrated study to understand marine biology, ecology, and evolution. It surveys the state-of-the-art, identifies challenges such as bridging model systems with global approaches, discusses potential economic/sociological/environmental impacts (with terrestrial comparisons), and calls for technological/conceptual advances and community collaboration without presenting new data, derivations, or tested hypotheses.

Significance. If the framing holds, the paper could help coordinate research efforts around host-microbe interactions in marine systems by cataloging open questions and emphasizing integrated study, with potential to influence how evolutionary and ecological questions are posed. Its contribution is programmatic rather than empirical; strengths include explicit identification of challenges and cross-system comparisons, but impact depends on community uptake rather than internal validation.

minor comments (2)

[Abstract and Introduction] The definition of 'long-lasting relationship' and 'coherent biological and functional unit' (stated in the abstract and introduction) remains high-level; adding one or two concrete operational criteria or examples from the surveyed literature would improve clarity without altering the perspective nature of the work.
[Future directions] The section on future directions calls for bridging 'functional research on simple and tractable model systems and global approaches' but does not specify any particular metrics or study designs that would constitute such bridging; a short illustrative paragraph would strengthen the call to action.

Simulated Author's Rebuttal

0 responses · 0 unresolved

We thank the referee for their positive assessment of our community perspective paper and their recommendation to accept. The referee's summary accurately captures the manuscript's scope, intent, and lack of new empirical data.

Circularity Check

0 steps flagged

No significant circularity detected

full rationale

The manuscript is a community perspective paper that defines the holobiont concept, surveys existing literature and open challenges, and advocates for integrated study of hosts and microbiota. It contains no equations, derivations, predictions, or empirical claims whose validity could reduce to fitted parameters, self-referential definitions, or load-bearing self-citations. The central stance is programmatic rather than mechanistic, with no load-bearing steps that collapse by construction to the paper's own inputs.

Axiom & Free-Parameter Ledger

0 free parameters · 0 axioms · 0 invented entities

This perspective paper relies on the pre-existing holobiont concept from prior literature without introducing new free parameters, axioms, or invented entities. No empirical fitting or mathematical derivations are performed.

pith-pipeline@v0.9.0 · 5964 in / 1099 out tokens · 46781 ms · 2026-05-24T22:52:03.962649+00:00 · methodology

discussion (0)

Lean theorems connected to this paper

Citations machine-checked in the Pith Canon. Every link opens the source theorem in the public Lean library.

IndisputableMonolith/Foundation/AbsoluteFloorClosure.lean; IndisputableMonolith/Cost/FunctionalEquation.lean reality_from_one_distinction; washburn_uniqueness_aczel unclear

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unclear
Relation between the paper passage and the cited Recognition theorem.

The holobiont concept ... posits that a host and its associated microbiota, living together in a long-lasting relationship, form the holobiont, and have to be studied together, as a coherent biological and functional unit

What do these tags mean?

matches: The paper's claim is directly supported by a theorem in the formal canon.
supports: The theorem supports part of the paper's argument, but the paper may add assumptions or extra steps.
extends: The paper goes beyond the formal theorem; the theorem is a base layer rather than the whole result.
uses: The paper appears to rely on the theorem as machinery.
contradicts: The paper's claim conflicts with a theorem or certificate in the canon.
unclear: Pith found a possible connection, but the passage is too broad, indirect, or ambiguous to say the theorem truly supports the claim.